Predation of cassowary dispersed seeds: is the cassowary an effective disperser?

Predation of cassowary dispersed seeds: is the cassowary an effective disperser?

168 © 2011 ISZS, Blackwell Publishing and IOZ/CAS ORIGINAL ARTICLE Predation of cassowary dispersed seeds: is the cassowary an effective disperser? Matt G. BRADFORD and David A. WESTCOTT CSIRO-Sustainable Ecosystems, Tropical Forest Research Centre, Atherton, Queensland, Australia Abstract Post-dispersal predation is a potentially significant modifier of the distribution of recruiting plants and an often unmeasured determinant of the effectiveness of a frugivore’s dispersal service. In the wet tropical forests of Austra- lia and New Guinea, the cassowary provides a large volume, long distance dispersal service incorporating benefi- cial gut processing; however, the resultant clumped deposition might expose seeds to elevated mortality.

We exam- ined the contribution of post-dispersal seed predation to cassowary dispersal effectiveness by monitoring the fate of 11 species in southern cassowary (Casuarius casuarius johnsonii Linnaeus) droppings over a period of 1 year. Across all species, the rate of predation and removal was relatively slow. After 1 month, 70% of seeds remained intact and outwardly viable, while the number fell to 38% after 1 year. The proportion of seeds remaining intact in droppings varied considerably between species: soft-seeded and large-seeded species were more likely to escape removal and predation.

Importantly, across all species, seeds in droppings were no more likely to be predated than those left undispersed under the parent tree. We speculate that seed predating and scatter-hoarding rodents are responsible for the vast majority of predation and removal from droppings and that the few seeds which undergo secondary dispersal survive to germination. Our findings reinforce the conclusion that the cassowary is an impor- tant seed disperser; however, dispersal effectiveness for particular plant species can be reduced by massive post- dispersal seed mortality.

Key words: Australia, Casuarius casuarius, disperser effectiveness, secondary dispersal, seed shadow. Correspondence: Matt Bradford, CSIRO, PO Box 780 Atherton, Qld, 4883, Australia. Email: ment. Dispersal and disperser effectiveness traditionally in- corporate both quantity and quality components of seed dis- persal (Schupp 1993). The quantity component is concerned with the number of seeds dispersed while the quality com- ponent deals with the treatment of the seed by dispersers, seed deposition, and the consequences for subsequent sur- vival and germination. As germination rarely occurs imme- diately after deposition, the processes that act upon a seed after initial dispersal make a critical contribution to dispersal and disperser effectiveness.

Pre-dispersal and post-dispersal predation have a mas- sive influence on the probability of a seed surviving to germination. Evidence suggests that seed predators de- INTRODUCTION Seed dispersal is a fundamental process in the dynamics of tropical forests. For fleshy-fruited plants, dispersal is largely a product of the foraging patterns of frugivores and the associated movement and deposition of the seeds. However, for effective or realized dispersal to occur, a seed must survive to germination and, ultimately, to establish- Integrative Zoology 2011; 6: 168-177 doi: 10.1111/j.1749-4877.2011.00242.x

169 © 2011 ISZS, Blackwell Publishing and IOZ/CAS Predation of cassowary dispersed seeds stroy the majority of seeds in many plant communities around the world (e.g. Janzen 1971; Blate et al. 1998; Vander Wall 2001). High levels of post-dispersal preda- tion might counter any perceived benefits of dispersal, such as movement away from a parent, handling effects and deposition pattern (Traveset et al. 2007) or improved location (Harper 1977; Schupp 2007). The extent of seed predation experienced by a plant is determined by a range of extrinsic and intrinsic factors. Primary extrinsic determinants of the level of predation experienced include predator type present and predator densities (Donatti et al.

2009). Both of these factors are determined by habitat type (Osunkoya 1994) and other environmental variables at a site (e.g. Lord & Kelly 1999; Zelikova et al. 2008). The type of predators present also determines whether dispersed seeds are most likely to be predated or secondarily dispersed (Harrington et al. 1997; Seufert et al. 2010). Although secondary dispersal will generally result in little significant change in dispersal distances (e.g. Forget 1990; Theimer 2001), it might or might not result in improved survival for seeds (Schupp 1988; Willson 1988).

Intrinsic determinants of seed fate include seed size and morphology. We might expect that the larger the reward offered by a seed, the greater the probability that it would be subject to secondary dispersal or predation. This would sug- gest that large seeds would be favored by secondary dis- persers and predators (Forget et al. 1998; Theimer 2003). Large seeds can be predated upon by all predator sizes, but are limited to being secondarily dispersed by larger animals. However, small seeds are easily moved by a greater range of animals, including invertebrates (Levey & Byrne 1993; Andresen 2001).

Seed fate, however, is likely to be at least partly dependent on energy and nutritive values of the seed (Vander Wall 2001; Briones-Salas et al. 2006). For some traits, it is easier to generalize. For example, hard-seeded species generally have an induced dormancy (Hopkins & Graham 1987) and, consequently, must persist longer at a site than soft-seeded species before germination occurs. Therefore, hard-seeded species are generally exposed to seed mortality factors for longer periods.

Rates of post-dispersal predation and secondary dis- persal are also potentially influenced by the deposition pattern of the disperser (Kwit et al. 2007). Some dispers- ers scatter seeds, either by depositing seeds individually as they move or in a manner that results in the seeds set- tling individually (e.g. from a height such that dung is dispersed as it falls). Others leave large clumps of seeds surrounded by fecal material. These contrasting patterns might result in different probabilities of predation and re- moval (Andresen & Levey 2004; Russo 2005), largely because of the relative ease with which individual versus large clumps of seeds are detected by a predator or disperser.

Although deposition pattern might have an effect, other factors, such as availability of other seeds, will influence the strength of this effect (McConkey 2005). Three species of cassowary reside in the closed forests of northern Australia and New Guinea. All of these spe- cies are fruit specialists and are considered important as seed dispersers. The relatively long gut passage time and ability to move large distances in search of food result in large dispersal distances for plants in its diet (Mack 1995; Westcott et al. 2005). Despite the cassowary’s relatively gentle gut processing of seeds, it has been shown to alter the germination success of individual seeds of some plant species (Lamothe et al.

1990; Webber & Woodrow 2005; Bradford & Westcott 2010). Across a broad spectrum of fruit and seed types, however, cassowary gut passage has no net effect on probabilities of survival or germination (Bradford & Westcott 2010).

Although cassowary gut-passage has little effect on individual seed germination, cassowaries deposit seeds in large clumps that might contain thousands of seeds. This deposition pattern, along with surrounding fecal material, can reduce seed germination success for some species (Bradford & Westcott 2010). Furthermore, it is possible that deposition in large clumps with fecal mate- rial might result in a greater signal to potential predators and, therefore, might influence seed predation rates. Currently, there is no information on seed survival through to germination in clumped cassowary droppings.

In this paper, we investigate whether the beneficial effects of large volume, long distance dispersal and gut processing are outweighed by any negative effect of seed predation and removal of cassowary dispersed seeds.

Specifically, our study examines the dispersal effec- tiveness of the southern cassowary (Casuarius casuarius johnsonii Linnaeus) in the Wet Tropics of Australia. In northern Australia, the species consumes large amounts of fruit from a wide range of species (Westcott et al. 2005), including a high proportion of large-seeded species (Bradford et al. 2008). We quantify the probability that a seed will be predated or secondarily dispersed from cas- sowary droppings before germination and compare these results to those for single seeds below, or adjacent to, par- ent trees. Using previously published studies, we specu- late on the vectors responsible for predation and second- ary dispersal of the seeds in the Wet Tropics of Australia.

Although we conclude cassowary dispersal to be effective, when predation and secondary dispersal are considered,

170 © 2011 ISZS, Blackwell Publishing and IOZ/CAS we predict that effective dispersal kernels (sensu Schupp 1993) will differ significantly from our current understand- ing of cassowary-produced dispersal kernels (Westcott et al. 2005; Dennis & Westcott 2007). MATERIALS AND METHODS Study site and species We conducted the study in intact rainforest in Wooroonooran National Park, on the eastern edge of the Atherton Tablelands, North Queensland,Australia (17°22’S, 145°45’E). The study area ranges from 600 to 700 m in altitude. Dominant forest types are complex mesophyll vine forest on basalt and simple notophyll vine forest on metamor- phics.

The southern cassowary (Casuarius casuarius johnsonii) is a large flightless bird, residing in northernAus- tralia and the southern lowlands of New Guinea. InAustralia, it primarily occurs between Townsville and Cooktown, with additional populations on CapeYork. It is a resident of closed forest but is known to use adjacent seasonally inundated swamps, woodland, mangroves and agricultural land. Experimental procedure Between March 1998 and July 2000, we located re- cently deposited (less than 7-day-old) intact cassowary droppings on, and adjacent to, lightly used research trails within the study area.

The network of trails was approxi- mately 12 km in length within a study area of approxi- mately 10 km2 . The trails, which are little more than in- distinct tracks, are unlikely to influence predator behavior. Droppings were chosen for monitoring if they showed no outward signs of disturbance, predation or seed removal. The fruit, endocarps or seeds (henceforth referred to as seeds) were identified and counted with minimal distur- bance to the dropping. Seeds were monitored each month and assessed as either: (i) intact and viable; (ii) predated; (iii) removed; (iv) rotted; or (v) germinated.

Seeds with the endocarp penetrated by either vertebrate or inverte- brate predators and rendered unviable were recorded as predated. Predated seeds were left in the dropping. Ger- minated seeds were left in the droppings and for the analy- sis were considered to be intact until the end of the study. All species were monitored for 12 months, with the exception of Castanospora alphandii (F.Muell.) F.Muell., which was monitored for 6 months due to its late fruiting in the study.

To identify any influence of seed characteristics on pre- dation and removal, we documented each species’ seed hardness, seed size and residual flesh adhering to the seed after gut passage. Seed hardness was scored using the categories of Blate et al. (1998): soft, able to be punc- tured by a fingernail; firm, able to be penetrated by a knife; and hard, not able to be penetrated by a knife. Seed size was scored as large (>8 mL volume), medium (1–8 mL) and small (

171 © 2011 ISZS, Blackwell Publishing and IOZ/CAS Only large and medium-seeded species were monitored in our study.

Residual flesh was scored as either all flesh stripped or minimal flesh stripped and was assessed by one author (MB) to ensure consistency. Four species commonly found in both cassowary drop- pings and as fruiting trees in the area, Aceratium doggrellii C.T.White, Acmena divaricata Merr. and L.M.Perry, Elaeocarpus grandis F.Muell. and Prunus turneriana (F. M.Bailey) Kalkman, were chosen to assess the fate of seeds in 2 control treatments. The control treatments were: (1) single undispersed fruits located under the canopy of parent trees, and (2) single fruits placed beyond the canopy of parent trees.

For control 1, fruiting trees of the 4 spe- cies were chosen and ripe fallen fruits were haphazardly located and marked in situ (see below) under the canopy. Fruit of the same species within a 20 cm radius were removed. For control 2, fruits were placed at distances of 10, 20, 30, 40 and 50 m from the edge of the projected canopy of each control tree at each of the cardinal com- pass directions. Fruits from the control treatments were not placed within 100 m of another conspecific fruiting tree. Difficulties in locating fruiting trees or fruit during the study limited us to 2 trees of each species and we aimed for 20 fruits in each control treatment per tree.

However for A. divaricata and A. doggrellii, this was not possible due to low fruit numbers or the presence of other conspe- cific fruiting trees immediately adjacent. Species attributes and treatment details are provided in Table 1. To aid in relocating the fruit, a 10 cm length of dental floss was glued to the fruit, and a plastic tag was inserted into the soil 10 cm from the fruit. The single fruits were revisited monthly and the fate of each was assessed in the same manner as the seeds in the droppings. Fruit moved but still with the dental floss attached and those located within 20 cm of the original placement were considered to be present.

The control treatments were monitored for 6 months.

Data analysis Only droppings that were dominated by 1 species (see Bradford et al. 2008) were used in the analysis. In addition, droppings were considered only if they had more than 10 seeds of the dominant species. This limited the number of droppings to 38 (Table 1). Because at each time period, including the final time period, seeds could be predated, removed, rotted, germinated or intact, we used survival analysis to test for the effect of seed traits and control treatments, and for relationships between traits or treat- ments and survival time. Survival analysis is appropriate in circumstances where the dependent variable represents time to a terminal event (e.g.

time to seed mortality), but where not all experimental subjects will achieve that event in the timeframe of the experiment, that failure is still of interest (Statsoft 2005). For example, in the present study, some seeds were still alive, either as seeds or seedlings, after 12 months, when the study had to be terminated. Predated, removed and rotted seeds were coded as com- Figure 1 Mean proportion (±1 SE) of seeds remaining intact (, Y left axis) and cumulative mean proportion (±1 SE) of seeds predated , removed () and rotted () across all species (Y right axis).

Predation of cassowary dispersed seeds

172 © 2011 ISZS, Blackwell Publishing and IOZ/CAS plete (i.e. dead), whereas germinated and intact seeds were codedascensored(i.e.stillaliveattheendoftheexperiment). To test for differences between the categories of seed traits, we used Cox’s F-test, and to test for an effect of time on the relationship between survival time and a trait, we used proportional hazard regression. This method makes no assumptions about the underlying hazard rate distribution but rather assumes that this is a function of the dependent variables (Statsoft 2005).

The model for the hazard of the ith individual under a given treatment is estimated as Hi(t) = h0 (t)*exp( *z1 ), where h0 (t) is the baseline hazard when independent variables equal zero, t is the respective survival time and z is the vector of individual cases. To reduce the effect of the small number of droppings for some species, comparisons within seed traits were under- taken on the basis of seed hardness, size and residual flesh categories, and not by species.

RESULTS Fate in droppings: across species The 11 species used in the analysis are presented in Table 1 along with seed attributes and details of treatments. From an initial 2342 seeds present in 38 droppings, the mean proportion of intact (germinated and ungerminated) seeds was 70% after 1 month and 38.5% at the end of the study period (Fig. 1). After 12 months, a mean of 23.4% of seeds were predated and left in the droppings, 34.6% were removed, and 3.5% rotted. Figures 2 and 3 show the percentage of seeds intact, predated, removed and rotted for each species. For the 11 species, total germination reached 14.8% by 12 months.

Fate in droppings: effect of seed traits The 4 soft-seeded species attained maximum germination within2months,withtotalgerminationvaluesof:Beilschmiedia oligandra L.S.Sm. (100%), Diploglottis bracteata Leenh (100%),C.alphandii(64%)andCryptocaryaoblataF.M.Bailey (68%). The only firm-seeded species (A. divaricata) attained maximum germination after 6 months, with a total germination of 63%. Calophyllum costatum F.M.Bailey was the only hard- seeded species to show germination (2% at 2 months). Consequently, there was an effect of seed hardness on survival (Cox’s F(358,2914) = 3.64, P < 0.001) with soft-seeded and firm- seeded species remaining intact longer than hard-seeded species.

Figures 2 and 3 show the fate of seeds in the 3 seed hardness categories. Seed size and residual flesh also showed a significant effect on survival, with larger seeds remaining intact longer (Cox’s F(218,3054) =2.63,P

173 © 2011 ISZS, Blackwell Publishing and IOZ/CAS Wald statistic = 15.26, P < 0.001). It should be noted that soft-seeded and firm-seeded species in our study are sig- nificantly larger than hard-seeded species (t = –2.88, df = 9, P = 0.018). Despite this, these effects remain significant even when included together in the proportional hazard regres- sion analysis. Comparison of droppings and controls For the 4 control species combined, the proportion of in- tact seeds remained higher in droppings than in the controls at all time periods (Fig. 4); however, this was not a signifi- cant difference (χ2 = 0.03, df = 1, P = 0.86).

The 4 species individually showed varied treatment effects in the number of seeds surviving (i.e. intact or germinated). None of the seeds of E. grandis remained intact in either the control treat- ment or in droppings for 1 month. Seeds of A. doggrellii showed no difference in survival between controls and droppings ( = 0.05, exp = 1.05, SE = 0.16, χ2 = 0.1, df = 1, P = 0.76). Seeds of A. divaricata ( = 1.03, exp( ) = 2.81, SE = 0.21, χ2 = 25.76, df = 1, P < 0.001) survived longer in droppings than both controls, while seeds of P. turneriana survived longer under and away from the par- ent than in droppings – 0.39, exp = 0.68, SE = 0.10, χ2 = 15.3, df = 1, P < 0.001).

DISCUSSION Despite sometimes significant levels of predation expe- rienced by seeds in cassowary droppings, our work shows that the cassowary is an effective seed disperser. Across the 11 species tested, 38% of seeds were left intact in the drop- pings after 1 year, with 15% of these having germinated. Two species, E. grandis and P. turneriana, showed little or no survival to 1 month, with interim observations suggest- ing that these seeds probably did not survive intact more than a few nights. Rates of seed predation and removal might vary with forest type, altitude and season. For example, while we recorded complete and rapid predation of E.

grandis seeds, Stocker and Irvine (1983) report seedlings of the same species emerging from an old cassowary dropping. Most importantly, only 1 of the 4 species for which control com- parisons were available, P. turneriana, experienced higher predation levels in droppings than in undispersed seeds or those dispersed adjacent to parent trees. In addition, seeds consumed and deposited by the cassowary will generally be dispersed further from the parent than if dispersed by other animal vectors (Westcott & Dennis 2007), with generally positive effects on germination success (Bradford &Westcott 2010).

For large-seeded species, the absence of other ani- mals capable of dispersing and internally processing their seeds in Australia means that cassowary dispersal, no mat- ter how effective, will be beneficial.

Our study shows that the clumped nature of cassowary seed deposition has no detrimental effect on seed survival. The small number of replicate trees achieved in this study means that these results alone should not be considered as conclusive. However, the concordance with other stud- ies from the region documenting comparable rates of single Figure 3 Fate of hard-seeded species in cassowary droppings after 30, 180 and 360 days. Fates are intact , predated ( ), removed , and rotted . d = number of droppings, n = number of seeds. Seeds germinated are considered to be still intact regardless of their fate after germination.

Predation of cassowary dispersed seeds

174 © 2011 ISZS, Blackwell Publishing and IOZ/CAS seed removal (Osunkoya 1994; Harrington et al. 1997) supports our conclusion. This result is not dissimilar to other studies where high densities of dispersed seeds are found, such as in clumped deposition by large dispersers (e.g. Pizo & Simao 2001; Andresen 2002) or the deposi- tion of seeds at latrines (Fragoso 1997). This result might be negated in some cases by the effect of seed clumping on germination success, which is generally seen as a nega- tive for the cassowary (Bradford & Westcott 2010) and other frugivores (Travaset et al. 2007).

Similarly, germi- nation in clumps might ultimately lead to reduced root and shoot development due to competition at later stages of growth (Pizo & Simao 2001) or increase the attraction to herbivores and pathogens.

There are few published studies on post-dispersal preda- tion and secondary dispersal in the wet tropical forests of Australia and certainly there is an absence of work on cas- sowary dispersed seeds. However, we can speculate on the agents of seed removal and mortality. Coprophagy is some- times practiced by cassowaries immediately after deposi- tion (Mack & Druliner 2003; M. Bradford, pers. observ.) but was not considered in our study because we began moni- toring the droppings 1–7 days after deposition. Webber and Woodrow (2005) report a high incidence of mortality of a soft-seeded species, Ryparosa sp.

nov. 1, in cassowary drop- pings due to fruit flies. We did not document insect damage to our seeds; however, we assume it was insignificant, as a large proportion of our soft-seeded species survived to germination. Previous studies (Osunkoya 1994; Harrington et al. 1997; Thiemer 2001; Dennis et al. 2004) have shown that a large proportion of the seed removal and predation in the study area is due to the actions of scatter-hoarding and predatory mammals. Although there are possibly 5 species of ground dwelling mammals able to consume high propor- tionsoffruitandseedsintheregion(Dennis2003),thewhite- tailed rat (Uromys caudimaculatus Krefft) is likely respon- sible for the largest proportion of the predation and seed removal from the droppings.

The species is common (Laurance & Grant 1994; Harrington et al. 1997) and is known to inflict high rates of mortality on the seeds of nu- merous rainforest species (Harrington et al. 1997; Theimer 2001).Although the white-tailed rat is probably responsible for the bulk of predation and seed removal, other rodents, feral pigs, musky rat-kangaroos, litter disturbance by ground foraging birds and abiotic factors, such as gravity and over- land water movement, probably also contribute to a lesser extent.

For effective or realized dispersal to occur, a seed must remain intact and viable until germination and then establishment. In comparison with soft-seeded species, spe- cies with a hard seed coat or endocarp were generally more heavily predated or removed by the end of 12 months, a period generally shorter than their time to germinate (Table 1; Figs 2 and 3). Exceptions were Halfordia kendack (Montrouz.) Guillaumin, the seeds of which rotted, and Elaeocarpus ruminatus F.Muell., the seeds of which prob- ably avoided heavy predation because of their small size. This rate and magnitude of loss is comparable to other stud- Figure 4 Mean proportion of seeds (±1 SE) remaining intact in droppings ( ), singly under parent trees ( ) and sin- gly beyond the canopy of parent trees ( ) for the species Aceratium doggrellii, Acmena divaricata, Elaeocarpus grandis and Prunus turneriana combined.

M.G. Bradford and D.A. Westcott

175 © 2011 ISZS, Blackwell Publishing and IOZ/CAS ies involving hard-seeded species in Australian wet tropical forests (Osunkoya 1994; Harrington et al. 1997; Thiemer 2001). Considered alone, this suggests that hard-seeded fruit are disadvantaged by cassowary deposition; however, pre- dation and removal rates from droppings were similar or lower than for undispersed seeds (Fig. 4). In contrast, the soft and firm seeds remained relatively intact throughout the study, before and after germination. Before germination, seeds without mechanical defenses tend to be targeted by invertebrate predators (e.g.

Sharma & Amritphale 2008; Kupruwicsi & Garcia-Robledo 2010) and are generally less preferred by vertebrate predators due to chemical defenses (Blate et al. 1998; Grant-Hoffman & Barboza 2010) or lower nutritional content (Vander Wall 2001). Post-germination, the altered chemical and nutritive state and functional mor- phology of cotyledons will largely determine if the cotyle- dons and seedling is predated.All soft-seeded species in our study exhibit hypogeal germination, resulting in cotyledons being less nutritious and more redundant for seedling sur- vival with time. Although differential patterns of fruiting and predator satiation might influence relative removal rates, the low predation of soft-seeded species seen in our study is the result of minimal enforced dormancy in soft-seeded spe- cies (Hopkins & Graham 1987), resulting in short times to germination and reduced exposure to post-dispersal seed predation.

The fact that cassowary gut passage results in increased germination success for softer seeds (Bradford & Westcott 2010) only adds to this advantage.

Approximately 36% of all seeds and 39% of seeds with hard endocarps in our study were removed from the droppings. In all cases their ultimate fate is unknown. These seeds will be subjected to 1 of 3 fates: (i) predated immediately; (ii) cached to die at a later date, either through predation or some other mortality factor; or (iii) cached to eventually germinate. Studies in the wet tropical rainforests of Australia suggest that very few seeds of any species re- moved by seed predators survive caching to germination. Theimer (2001) found that none of 61 seeds of the hard, large-seeded Beilschmiedia bancroftii (F.M.Bailey) C.T.

White survived caching by white-tailed rats. Similarly, of almost 1000 cached seeds of 3 hard, large-seeded species (Harrington et al. 1997), all but a few were eaten within several weeks, with the longest surviving uneaten to 125 days. Evidence also suggests that seeds are not taken far before being cached (Theimer 2001), so dispersal distances of any surviving seeds are not significantly altered. In demonstrating the magnitude of predation and re- moval of seeds from cassowary droppings, we have shown that across all species a cassowary dispersed seed has a similar probability of survival to germination than if it remains undispersed close to the parent.

This result sug- gests that any Janzen-Connell effects (Janzen 1970; Connell 1971) that are likely to come into play do so after the seed stage and during the establishment phase. Consequently, the cassowary must be considered an ef- fective disperser as the long distance and large volume movement of seeds combined with a generally positive gut processing effect negate any detrimental effect that a clumped deposition pattern might have on seed germina- tion and seedling survival. Due to high seed mortality for particular species, our results also show that the incorpo- ration of predation and secondary dispersal of deposited seeds is essential in the generation of effective, or realized, dispersal kernels.

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Predation of cassowary dispersed seeds

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