by Dr Len .Martin, Department of Physiology and Pharmacology, The University of Queensland and Allen McIlwee, School of Tropical Biology James Cook University.

Population dynamics, calculated from the limited reproductive potential of Pteropus spp., show that imposed-mortalities as low as 10% per annum, added to a species’ natural mortality, will push large populations into rapid decline. Current death-rates in a single Queensland orchard will halve P. conspicillatus populations ranging in size from 100,000 - 200, 000 in about 5 years. The proposed culling of 20,000 P. poliocephalus in the Melbourne Botanic Gardens (MBG) will have significant adverse effects.

We predict that continuation of the seasonal culling of P. conspicillatus at the rates estimated to occur in one Queensland orchard will lead to rapid declines in populations of P. conspicillatus as large as 50,000 to 800,000, the most likely estimate being over 200,000. Furthermore, because of the mobility of P. conspicillatus, the impact of persistent culling and resultant population decline will spread and endanger the species throughout the Wet Tropics World Heritage Area. Similarly, an ongoing culling of P. poliocephalus in the MBG will not only compromise populations in Victoria, but also in NSW and Queensland and, by adding to the severe mortality burden already imposed on this species by orchard kills, put the species at risk.

In relation to the N. QLD court case, a flying-fox researcher maintained that it is difficult to gather scientifically valid estimates of the sizes of flying fox populations, and argued that since, in his view, there were no valid estimates of P. conspicillatus population sizes in the vicinity of the orchard in question, there was no scientific evidence that orchard electrocutions of P. conspicillatus would cause any significant decline in local or more wide-spread populations or have any significant impact on the Wet Tropics World Heritage Area.

However, as well as ignoring the precautionary principle, this advocacy of continuing electrocution ignored the scientifically established facts of the low reproductive potential of P. conspicillatus, and the sensitivity of the species to population decline, under any imposed-mortality, whether by electrocution, shooting, poisoning, or roost destruction. It seems that proponents of the MBG culling of P. poliocephalus are likewise ignoring the precautionary principle, and the sensitivity of this species to any imposed-mortality.

Such imposed-mortality occurs in and around many orchards and townships in Queensland, NSW and Victoria. Thus, while we emphasise quantitative estimates based on the imposed-mortality rates of P. conspicillatus in a single Queensland orchard, such deaths cannot be regarded in isolation. They are a significant contribution to a massive on-going mortality imposed on this species. Not only will this particular orchard culling of a perceived "local" population fail to eradicate attacks upon the orchard, but the killings "vacuum effect", where the local population is maintained only through immigration of animals from far a field So too will the culling of P. poliocephalus in the MBG fail to eradicate the problem, but will draw more and more animals into the killing fields from far afield.

One may define "historic" mortality as the "natural" mortality experienced by Pteropus spp. in effectively undisturbed habitat prior to European settlement. In the calculations described below, a 10% per annum death rate and 90% breeding success of adult females are realistic assumptions for "historic" mortality and fecundity (see Martin and McIlwee, 2001).

One may define "modern" (increased) mortality as that experienced by Pteropus spp. subsequent to European settlement, and resulting from "unintentional" causes such as widespread destruction of habitat, reduced food sources, less-than-optimal maternity roost sites, micro and macro climate change, extreme "stochastic" climate events etc. Adverse factors that increase mortality are also likely to decrease fecundity. On the basis of discussions with colleagues, published death rates and population models based on the minimum rates of decline in P. poliocephalus and P. conspicillatus (details cited in Martin and McIlwee, 2001) "modern" annual death-rates could well average out at 20-35% deaths per year with fecundity rates as low as 70-80% for adult females. For example, Vardon and Tidemann (1998; 2000) in field studies of P. alecto, found 30% of adult females were non-breeding while juvenile survival rates were extremely low, as little as 43% for females. They calculated that only "approximately one in three females born lives to adult size and reproduces".

One may define "imposed-mortality", as that due to intentional, flying-fox-specific causes such as electrocution, shooting, poisoning, maternity-roost disturbance or destruction. Such imposed-mortality is likely to be age independent. The effects of any imposed-mortality on population decline are likely to be additional to the "natural" 10% mortality whether this be historic or modern (Martin and McIlwee, 2001).

Pierson and Rainey, in their (1992) review of flying-fox biology, make the point that flying-foxes, "have relatively few predators other than man" and state that, "Though information on age structure and estimates of age-specific mortality rates for Pteropus are lacking, the long life span and low reproductive rate clearly indicate animals with an evolutionary history involving low levels of natural mortality". The obvious corollary of this is that unusually high levels of mortality, either natural or un-natural, will lead to species decline. The question addressed in this report is, how rapid a decline?

Values for age-specific-fecundity (m_x) are based on those observed in captive colonies, and from samples taken from the wild (Ratcliffe 1932; Martin et al. 1996). Thus m_x = 0 for the first year of life of a female, 0 or 0.1 for the second year and remains constant thereafter to year 15, at values ranging from 0.5 (100% of females rear 1 young to independence each year) to 0.375. A neonatal sex-ratio of 1 is assumed for the whole of a female’s reproductive life, and since only females produce offspring, the maximum m_x is 0.5. The death-rates used lead to a relatively small proportion of animals surviving to 15 years. In all of these calculations, it is assumed that all females older than 15 years die or are infertile. A cut-off at 15 years is not incompatible with the species’ longevity in captivity, and Tidemann’s 1999 claim that, "a maximum age of 10-15 years seems possible". The oldest flying fox recovered from the wild after banding was a female P. poliocephalus found dead in August 2000, and estimated by Tidemann to be 12.8 years old when it died. Since Pteropus are seasonal breeders, and births effectively occur close to each maternal birthday, the values of x refer to end of each year of a cohort’s life.

Figure 1 illustrates some of these cases. It shows how cohorts of a thousand new-born bats, increase or decrease exponentially with time (years) in the relationship N_t = N₀.e^rm.t with various values of r_m. Because the changes are exponential (ie., geometric progressions) the results are plotted on a logarithmic scale which gives straight line relationships which are easier to interpret. The horizontal dotted lines show where each population first doubles - or halves.

In discussing death-rates with flying fox researchers and carers, most accept that a 10% per annum "natural" death-rate of adults is not unreasonable. However, all qualify their acceptance by placing it at the low end of the scale (Martin and McIlwee, 2001). In addition, flying foxes must contend with natural catastrophic events, such as droughts and heat waves that have the potential to cause large increases in mortality, particularly among juveniles. For example, in the late 1990s, in maternity roosts in Queensland and NSW, very high day-time temperatures and smoke caused deaths of large numbers of P. poliocephalus and P. alecto of all ages, but particularly juveniles, from dehydration and heat-shock. Hall (personal communication, 2000) observed mass abortions in camps of these species in SE Queensland; 2,000 out 12,000 females aborted near-term foetuses in Beenleigh in 1978; large numbers of aborted foetuses were observed in the Indooroopilly camp in 1983. Also Tidemann (1999) states for P. poliocephalus, "Notwithstanding the mobility (and adaptability)... large groups of animals sometimes perish, even in core areas of the range, during periods of widespread or extended food shortage". For P. conspicillatus in N. QLD, an on-going cause of high death-rates in both adults and juveniles has been infestations with ticks and subsequent paralysis (Mclean, personal communication, 2001). Our models make it clear that flying-fox populations can recover only slowly from such events.

It would seem our "natural" (i.e. pre-European) 90% fecundity and 90% survival baseline estimate is highly conservative, in the face of habitat destruction, natural stochastic events and direct exploitation by humans. Thus, we view "modern" baseline mortality rates in the range of 20-30% per annum as realistic. Likewise, given Vardon and Tidemann’s observation that 30% of adult female P. alecto sampled in the wild were non-breeding, "modern" fecundity rates as low as 70-75% are not unreasonable. These two adverse effects on populations (namely, high mortality and low fecundity) are also likely to be closely linked, such that changes in one will have a direct additive effect on the other.

Figure 1. Exponential increases and decreases in numbers of flying-foxes over 15 years under the effects of varying survival (S) and fecundity (F) rates.

A subsection of flying-fox researchers argue that it is difficult to produce scientifically valid estimates of flying-fox population sizes that are acceptable to all flying fox researchers. Though the effects of culling practices depend on the size of a population at risk, this "lack of knowledge" does not pose any obstacle to calculating, for example, the impact of observed deaths on local flying fox populations. This is because realistic estimates of natural mortality and fecundity can be used to work "back" from any known amount of culling to calculate the size of a population that would be put into rapid decline by such culling.

The basis for the following calculations are the same as those presented above, namely: all females are dead/ infertile after year 15; there is a "natural", age-independent death-rate; a constant age-independent adult fecundity; "imposed" death-rates are age-independent, and additive with the "natural" death-rate; processes associated with "imposed" death-rates do not affect fecundity. This last assumption may not be tenable, as will be evident in the discussion of electrocution. In calculating how big a population will go into serious decline in response to a given electrocution rate, we have used three "natural" death and fecundity rates: 10% annual natural mortality with 90% fecundity; 20% annual natural mortality and 80% fecundity; 25% annual natural mortality and 75% fecundity.

Table 2. The relationship between the natural mortality and fecundity of a flying-fox population, and the size of population that is put into rapid decline by a given killing rate. The 4 kill rates used are based on the current rate of killing adult female P. conspicillatus in one season in the one orchard: columns 1 & 2, respectively, assume 50 and 70% of counted dead are female; columns 3 & 4, are as for columns 1 & 2 but assume the counts underestimate deaths by 10%. The figures in brackets are the times to halve each population, in years.

However, the table does not take into account deaths of foetuses and neonates resulting from maternal deaths, or maternal injuries with consequent abortion, failure of lactation, rejection of young, etc. Allowing a fecundity rate of 70% in adult females [note here that, if the fecundity rate is higher, so too is the foetal/neonatal death rate], additional foetal and neonatal deaths arising from the four estimates of adult female deaths alone, are 7,408, 10,372, 8,149 and 11,409 respectively, and could well be higher. If these numbers represent 10% of a population, then populations experiencing an additional year 1 mortality of 10%, are calculated as respectively: 74,080; 103,720; 81,490; & 114,090.

Add this 10% "unperceived" kill of juveniles in this orchard to the adult mortality, and the most-likely size of population driven into rapid decline by the kill goes up accordingly. Thus we should be concerned about a decline in a population of more than 200,000 flying foxes, all within feeding range of the farm. Add the impact of generalised habitat destruction plus kills on electrocution grids in other orchards across the region, and it is easy to see how P. conspicillatus throughout the entire WTWHA may be at risk of extinction. Ten additional orchards with kill rates comparable to those cited above, and flying fox populations ten-times the size those calculated above will result in a rapid decline of 2,000,000 to 8,000,000 flying foxes - animals whose importance has been noted by Vardon and Tidemann (1998) who emphasised, "the vital role they play in maintaining ecosytems", as did Tidemann and Vardon (1997) who stated that: "flying foxes, by dispersing pollen and seeds, are pivotal to ecosystem maintenance".

(a) that, the proponents had failed to adequately substantiate the hypothesis that such culling of bats would solve the problem by preventing any flying-foxes from roosting in the MBG;

(b) that, the proponents had failed to adequately document likely outcomes;

(c) in particular, given the known mobility of the bats, the proponents had failed to take into account the likelihood of animals killed in the gardens simply being replaced by animals from further afield;

(d) that given the species' scientifically accepted vulnerable status, it would be unacceptable to slaughter so many bats on the basis of a dubious hypothesis.

Indeed, this view is supported by Tidemann (2000) who, in arguing that electrocution of P. conspicillatus in a N. QLD lychee orchard would not have significant adverse effects, stated that, "In any event, a localised reduction in numbers of spectacled flying-foxes is likely to be counterbalanced by individuals flying in from elsewhere. The mobility of spectacled flying foxes is unknown, but... satellite tracking studies of grey-headed flying foxes... have revealed one individual that flew 500 kilometres in less than a week. It is not known if spectacled flying-foxes have a comparable capacity for long-distance flight, but it is known that they are highly mobile animals". It surprises us that a similar view was not put forward by the proponents of the culling of P. poliocephalus in the MBG.

Let us expand on this. P. poliocephalus and P. conspicillatus may routinely forage over 50km per night. If there is a good food source, individuals will move from distant roost sites to ones closer to that food source. Similarly, if there is a good food source and bats from a local roost are being killed, bats from more distant areas will move into vacancies in that roost. Thus, to a grower or botanic gardens manager killing the animals, there will be a perception of "millions" of animals - a never-ending supply - and a misconception that the animals breed like rats and mice. The ecological term for such movement into a cull site is "source-sink dispersal" (Pulliam, 1996); the site of culling is the "sink" into which animals move from surrounding "source" areas. Vardon and Tidemann (2000) even suggest that such is likely to occur with P. alecto, "given the species’ high mobility", and they hypothesise that, "the source would be the north-eastern Australian range of P. alecto and the sink northern New South Wales and southern Queensland".

Thus, not only will any orchard or Botanic Gardens culling of a perceived "local" population fail to eradicate problem damage, but the killings will produce a population sink, a pteropucidal "black hole" which will drag animals into it from far afield. The image of a black hole and its irresistible gravitational force sweeping everything into its maw is a not unreasonable metaphor. The culling produces a local vacant niche, which then becomes occupied by animals moving into it from further afield, which are then killed, so producing a local vacant niche which then....and so on. It seems self-evident that the culling of P.conspicillatus in a single orchard will affect populations over a broad span of the surrounding Wet Tropics World Heritage Area. Similarly the culling of 20,000 P. poliocephalus in the Melbourne Botanic Gardens will draw other bats in and affect populations as far afield as NSW. Apropos the MBG, important questions remain. For how long does the MBG propose to continue culling? How many bats, in total, do they propose to kill?

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