Biological Conservation 144 (2011) 2282–2288

Contents lists available at ScienceDirect

Biological Conservation
journal homepage: www.elsevier.com/locate/biocon

Demonstrating decline of an iconic species under sustained indigenous

harvest – The pig-nosed turtle (Carettochelys insculpta) in Papua New Guinea
Carla C. Eisemberg a,⇑, Mark Rose b, Benedict Yaru c, Arthur Georges a
a
Institute for Applied Ecology, University of Canberra, ACT 2601, Australia
b
Flora & Fauna International, Jupiter House, 4th Floor, Station Road, Cambridge, CB1 2JD, UK
c
Oil Search Ltd., GPO Box 2442, Sydney, NSW 2001, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Papua New Guinea has astonishing biological and cultural diversity which, coupled with a strong
Received 7 February 2011 community reliance on the land and its biota for subsistence, add complexity to monitoring and conser-
Received in revised form 16 May 2011 vation and in particular, the demonstration of declines in wildlife populations. Many species of concern
Accepted 4 June 2011
are long-lived which provides additional challenges for conservation. We provide, for the first time, con-
Available online 29 June 2011
crete evidence of a substantive decline in populations of the pig-nosed turtle (Carettochelys insculpta); an
important source of protein for local communities. Our study combined matched village and market sur-
Keywords:
veys separated by 30 years, trends in nesting female size, and assessment of levels and efficacy of harvest,
Carettochelyidae
Population trends
each of which was an essential ingredient to making a definitive assessment of population trends. Oppor-
Management tunities for an effective response by local communities to these declines needs to consider both conser-
Exploitation vation and fisheries perspectives because local communities consider the turtle a food resource, whereas
Levels of harvest the broader global community views it as a high priority for conservation. Our study in the Kikori region
Female size is representative of harvest regimes in most rivers within the range of the species in Papua New Guinea,
and provides lessons for conservation of many other wildlife species subject to harvest.
Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction subsistence to a cash economy, increasing human population size

and the introduction of modern fishing and hunting techniques
Papua New Guinea (PNG) is one of 17 megadiverse countries (Bennett and Robinson, 2000). These changes can intensify the
that account for 70% of global biodiversity (Mittermeier et al., pressures placed on natural resources (Dudgeon et al., 2006;
1997). The biodiversity of many of these nations is under threat, Groombridge and Wright 1982; Rosser and Mainka, 2002) and
particularly in tropical countries that allow and encourage aggres- the outcome is often the decline and extinction of wildlife
sive mining, forestry and agricultural practices driven by immedi- populations.
ate financial imperatives rather than longer term sustainable Exploitation of long-lived species brings additional problems for
economic considerations (Laurance et al., 2001; Sodhi et al., conservation management (Marsh et al., 2004; Romero et al.,
2004). Papua New Guinea has remarkable species diversity and 2002). They generally exhibit slow growth and late maturity.
high levels of endemism. Its biodiversity is of international con- Reproduction is usually characterized by low fecundity (e.g. large
cern, and attracts considerable conservation funding in support cetaceans) or variable and infrequent recruitment (e.g. sea turtles)
of government initiatives to prevent overexploitation of their bio- (Musick, 1999). These characteristics make long-lived species par-
logical assets (Connell, 1997). ticularly vulnerable to excessive adult mortality (Broderick et al.,
Charting a path to a sustainable future is complicated by the 2006; Frazer, 1992, but see also Fordham et al., 2007, 2009). Fur-
equally astonishing cultural diversity of the Papuan human popu- thermore, the impact of exploitation younger life stages and trends
lation, many of whom still live traditional lives in villages distrib- toward population collapse may be masked because absence of
uted through the New Guinea highlands and coastal plains (Foley, recruitment can be concealed by the presence of long-lived senesc-
1986). This cultural diversity coupled with a strong community ing adults. Declines may progress for many years before it is
reliance on the land and its biota for subsistence, presents a detected and overcome (Browne and Hecnar, 2007; Musick, 1999).
number of challenges for monitoring and managing wildlife popu- Long-lived animals are important sources of protein for
lations. Wildlife management is complicated by a shift from indigenous communities and have been for many centuries
(Milner-Gulland and Bennett, 2003; Smith, 1979). The pig-nosed
⇑ Corresponding author. Tel.: +61 2 62015785; fax: +61 2 62015305. turtle (Carettochelys insculpta), an iconic species from the Kikori
E-mail address: eisemberg@aerg.canberra.edu.au (C.C. Eisemberg). region, is no exception (Georges et al., 2008a). It is of conservation

0006-3207/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2011.06.005
 C.C. Eisemberg et al. / Biological Conservation 144 (2011) 2282–2288 2283

concern because it is the sole survivor of a once widespread family Before interaction with Europeans, the lowland upstream sec-
(Carettochelyidae), because it has a restricted distribution, and be- tions of the Kikori River were characterized by a few sparsely-dis-
cause it is subject to intense harvest pressure (Groombridge and tributed small villages whereas the delta region had many villages
Wright, 1982). It is one of many chelonian species of international each with more than 1000 people (David, 2008). Nowadays, there
concern (Rhodin et al., 2011). are 51 villages and fishing camps, from three major language
Highly prized as food, these turtles are caught and their eggs are groups, distributed over much of the lowland area. The Rumu lan-
collected for consumption by local villagers or trade in local mar- guage group comprises approximately 700 people living in villages
kets (Georges et al., 2008a). Local villagers harvest C. insculpta eggs mainly in the limestone plains upstream of the main Kikori Town-
with close to 90% efficiency (Pauza, 2003). Growth in human pop- ship. The Porome language group comprises approximately 600
ulations, a greater propensity for villages to establish on riverbanks people residing in villages of the delta region. The Kerewo language
since tribal warfare ceased, and the introduction of new technolo- group is the largest, comprising approximately 1500 people whose
gies, particularly outboard motors, have brought added pressure to lands are in the deltas and coastal regions of the Omati and Kikori
turtle populations in recent decades. This has led to the wide- River systems. Each of these groups is subdivided into networks of
spread view that populations of C. insculpta have suffered severe clans and lineages with their own territorial estates (Busse et al.,
population declines (Georges et al., 2008b; Groombridge and 1993).
Wright, 1982; Pauza, 2003). There is however, remarkably little di-
rect evidence of these declines, and what there is remains unpub- 2.2. Methods
lished. The International Union for Conservation of Nature (IUCN)
listing of the species as vulnerable (IUCN, 2009) rests largely on a A daily survey of pig-nosed turtle eggs passing through the
precautionary approach to evaluation of its status. This uncertainty Kikori (7°240 44.4500 S; 144°140 51.7800 E) and Sirebi markets
has in turn led to reduced commitment to act to conserve the pig- (7°120 23 .3600 S; 144°140 47.8000 E) was conducted during the turtle
nosed turtle despite its international profile as a distinctive relic nesting seasons (September to February) in the years 1980–1981,
species. 1981–1982, 2007–2008, 2008–2009. Only the Kikori market oper-
Assessing the impact of small-scale or artisan fisheries in re- ated in the years 1980–1982. A second market was established at
mote locations of developing countries is extremely necessary be- the Sirebi Forestry Camp in 2007 and continued to operate until
cause of its value to local economies (Humber et al.,, 2010; Low early 2009. We based the comparisons among years on the Kikori
et al., 2009; Salas et al., 2007; Soykan et al., 2008; Townsend market in 1980–1982 versus the combined totals for both markets
et al., 2005). Nevertheless, few studies have the benefit of long in 2007–2009. Data recorders comprised volunteers from local vil-
term data (Broderick et al., 2006; Spotila et al., 2000). Furthermore, lages, who visited Kikori and Sirebi markets every day of operation
direct evidence of decline is very difficult to obtain. Indirect evi- and recorded the number of pig-nosed turtle eggs for sale and ob-
dence through market surveys typically span too few years to be tained estimates of counts of eggs that had already been sold. We
of value, and in any case can underestimate the extent of harvest regularly visited the markets to undertake spot surveys as a cross
(Milner-Gulland and Bennett, 2003). To eliminate some of these check on the veracity of the accounts from the recorders.
potential biases, it is necessary to combine market surveys with Two riverine villages (Kopi and Waira) and one coastal village
surveys of households and direct surveys of wildlife populations (Dopima) were selected for intensive monitoring of egg and turtle
(Milner-Gulland and Bennett, 2003). Thus, obtaining defensible numbers consumed in the 2007–2008 and 2008–2009 nesting sea-
evidence of decline in complex situations involving both human sons. These villages were selected because of comparable data col-
harvest, altering harvest practice and patterns of consumption lected there in the nesting season of 1981–1982. Data on
and environmental change presents a formidable challenge. household consumption was recorded by volunteer village resi-
In this paper, we meet this challenge with matched surveys of dents. Four volunteers in Kopi, two in Waira and one in Dopima
C. insculpta consumption via both market and village over almost visited all village families every week to access the number of eggs
30 years in the Kikori delta, which provide the first evidence of harvested per day. When shells or live turtles were available, we
population declines of this iconic species. We compared the nest- used a flexible measurement tape to measure the curved carapace
ing female size between the two periods to evaluate the effect of length (CCL).
selective harvesting of nesting females. We monitored the nesting Nest survival rate was recorded for the two most remote
survivorship in natural sandbanks to access the level of harvest nesting areas (Turuvio island and Wau creek sandbank) in the
pressure. Finally, we identify opportunities for an effective com- 2007–2008 and 2008–2009 nesting seasons. Data on nest fate were
munity level response to these declines with a view to establishing collected by local volunteers and validated by direct survey every
more sustainable harvest practices for this important food species. month. Nest characteristics (clutch size, egg diameter and hatch-
ling weight) were measured in all years. To ensure comparability
of data, only data from nesting females, nests, eggs, and hatchlings
2. Material and methods from nests laid in the riverine sandbanks in December were used
for the t-test comparisons between years. Price for the pig-nosed
2.1. Study site turtle meat and eggs was also recorded from villages and markets.
Data on egg diameter and hatchling weight were averaged by
The Kikori drainage extends from the coastal region and delta to clutch to avoid pseudoreplication arising from lack of indepen-
the limestone plains of the Kikori lowlands (Löffler, 1977) in the dence of eggs within clutches. Statistical tests followed those rec-
Gulf Province of Papua New Guinea (Fig. 1). The river system is ommended by Sokal and Rohlf (1981) and were performed using
highly confined within its limestone bed, and meanders and ox- SAS 9.1 or by hand. Chi-square tests were performed on counts
bows are absent. The delta is a large alluvial plain below 40 m ele- of clutches as the independent entities satisfying the underlying
vation, dissected by a tributary system of river channels, and multinomial assumptions. Where we had only egg counts, not
formed where thick layers of soils, principally soft silts and clays, clutch counts, the number of clutches was estimated by dividing
have been deposited over the underlying limestone plain. The coast the number of eggs by the average clutch size of 21.3, so that these
comprises the delta islands exposed to the Gulf of Papua. Wind and data could be included in the statistical analyses. We used the dif-
wave action creates coastal beaches, sand bars and sand islands in ference between the total number of eggs consumed (market and
what is a very dynamic system (Enesar Consulting, 2005). villages) in the 1981–1982 nesting season and the average from
2284 C.C. Eisemberg et al. / Biological Conservation 144 (2011) 2282–2288

Fig. 1. Map of the Kikori region showing permanent settlements (villages), temporary settlements (fishing camps) and markets. Areas with sandbanks, where Carettochelys
insculpta females lay their eggs, are delimited by dashed lines. The Kikori region is divided into delta, riverine (area upstream of the delta) and coast.

the total number of eggs consumed in the 2007–2008 and

2008–2009 nesting seasons to estimate the level of decline.

3. Results

The number of turtle eggs passing through the markets in

2007–2009 was substantially lower than in 1980–1982
(X2 = 269.04, df = 3, p < 0.0001; Fig. 2). The proportion of eggs sold
in market decreased from 28.5% (1980–1981) to 19.7.3%
(2007–2008) and subsequently to 8.4% in the next year
(X2 = 1704.29, df = 2, p < 0.00001; Fig. 3). However, fewer eggs
overall were consumed in the 2007–2008 and 2008–2009 nesting
seasons in the villages of Kopi (X2 = 72.67, df = 2, p < 0.0001), Waira
(X2 = 62.65, df = 2, p < 0.0001) and Dopima (X2 = 84.27, df = 2,
p < 0.0001) when compared with the numbers consumed in
1981–1982 in the same villages (Fig. 4). On the basis of these data,
our best estimate of the level of decline is 57.2% since 1981. Fig. 2. Number and percentage of pig-nosed turtle eggs passing through the active
markets of the Kikori lowlands (Kikori and Sirebi markets) in the nesting seasons of
Nest survival was exceptionally low on the nesting beaches of 1980–1981, 1981–1982, 2007–2008 and 2008–2009. There was a significant
Turuvio Island during the nesting seasons of 2007–2008 (3.3% of decline in trade between 1980–1982 and 2007–2009 (X2 = 269.04, df = 3,
120 nests survived) and 2008–2009 (2.9% of 104 nests survived) p < 0.0001).
 C.C. Eisemberg et al. / Biological Conservation 144 (2011) 2282–2288 2285

Table 1
Nesting female sizes, nest and market attributes for Carettochelys insculpta from the
Kikori region in the 1980–1982 and 2007–2009 nesting seasons.

Parameter 1980–1982 2007–2009 Trend

CCLa (cm) 58.2b ± 1.0 54.3 ± 0.7 (46.8–57.1, Decrease
(52.2–61.0, n = 9) n = 20)
Clutch size 22.8 ± 0.5 (11–33, 22.2 ± 0.6 (7–37, n = 93) Decrease
n = 73)
Egg diameter 4.37 ± 0.02 4.33 ± 0.02 (4.11–4.54, Decrease
(cm) (4.19–4.5, n = 25) n = 36)
Hatchling 30.10 ± 0.88 32.41 ± 1.10 (25.8–35.1, Increase
weight (g) (23.00–34.3, n = 11)
n = 17)
Egg price (Kina) 0.03 ± 0.00 0.49 ± 0.01 (0.40–0.50, Increase
(0.01–0.05, n = 8)
n = 128)
Turtle price 3.5 ± 0.2 23.8 ± 3.8 (10.0–55.0, Increase
(Kina) (1.0–5.0, n = 54) n = 12)
Fig. 3. Percentage and number of pig-nosed turtle eggs passing through the active
a
markets and villages of the Kikori lowlands (Kikori and Sirebi markets) in the CCL = curve carapace length.
b
nesting seasons of 1980–1981, 1981–1982, 2007–2008 and 2008–2009. There was Means are given with their SE, maximum and minimum sample values, and
a significant increase in percentage of eggs consumed in the villages between 1980– sample sizes.
1982 and 2007–2009 (X2 = 1704.29, df = 2, p < 0.00001).
from matched village and market surveys spanning 30 years,
trends in nesting female size, and assessment of levels of harvest,
all of which are essential to make a definitive assessment of the
population trends in this species.
Both village and market surveys are essential because the com-
bined data capture consumption in the villages, exchange among
local villagers, and informal sales in addition to formal trade
through markets (Milner-Gulland and Bennett, 2003) and so are
robust to shifts in patterns of consumption. Growth in human pop-
ulations can be expected to shift the balance between village con-
sumption and trade, and so can be expected to distort assessments
made on market surveys alone. Indeed, we demonstrated an in-
crease in the relative importance of consumption in villages over
market trade between 1981–1982 and 2007–2009, illustrating
the need to couple market sales with data on local village
Fig. 4. Number of pig-nosed turtle eggs consumed in the villages of Kopi, Waira and consumption.
Dopima in the nesting seasons of 1981–1982, 2007–2008 and 2008–2009. There
Perhaps more difficult to assess is the effect of shifting empha-
was a significant decline in consumption between 1981–1982 and 2007–2009.
sis from a subsistence economy to a cash economy as more villag-
ers come to engage in resource development through mining,
and Wau Creek 2008–2009 (2.0% of 100 nests) and did not differ forestry industries and associated infrastructure development, or
significantly among any monitored location (X2 = 0.37, df = 2, indeed employment in support of conservation efforts (Georges
p = 0.70). Humans were the only predator responsible for nest mor- et al., 2008a,b). The impact of a cash economy is a double-edged
tality in Turuvio Island while monitor lizards (Varanus indicus) sword. One cannot assume that economic development will reduce
uncovered and removed the eggs of 65% (n = 65) of the 100 nests demand for wild meat. The opposite could easily happen in the
in Wau Creek, with a further 33% (n = 33) harvested by humans. short term (Milner-Gulland and Bennett, 2003). In the presence
The average size of nesting females, clutch size and egg diame- of well established transport infrastructure and legal or illegal
ter was smaller in the 2007–2009 than in the 1980–1982 nesting trade networks, a cash economy can have devastating impacts on
season. On the other hand, egg and meat price increased and high profile species because of high returns and opportunities de-
hatchlings were heavier (Table 1). However, only the size of nest- rived from a global market (van Dijk et al., 2000).
ing females was statistically significant (t = 2.53, df = 16.2, The impact of such trade on native turtle populations because of
p < 0.05). Nesting females in 1980–1982 had an average curved high demand in China arising from the combination of traditional
carapace length 3.94 cm larger than in 2007–2009 (Fig. 5). Clutch practices and new found wealth is well documented (van Dijk
size (t = 0.91, df = 164, p = 0.36), egg diameter (t = 1.25, df = 52, et al., 2000). The initial stages of such trade in C. insculpta are seen
p = 0.22) and hatchling weight (t = 1.22, df = 21.3, p = 0.24) did in neighbouring Indonesia. International pet trade has largely dri-
not differ significantly between periods. ven the recently intensified egg collection in West Papua (Matur-
bongs, 1999; Shepherd and Nijman, 2007). The level of harvest
involved is unlikely to be sustainable, but there are no rigorous
4. Discussion monitoring programs in West Papua to assess the impact. This
trade is also affecting the exploitation and conservation status of
Reports over the last 30 years have suggested dramatic declines the species in PNG (Rhodin and Genorupa, 2000).
in C. insculpta natural populations in New Guinea (Georges et al., On the other hand, the global trade networks that have been
2008a,b; Groombridge and Wright, 1982; Pauza, 2003) but these established in West Papua (Samedi and Iskandar, 2000, 2002)
have largely derived from anecdotal information or inference and which extend across the border into the western province of
drawn from observations on the intensity of harvest. We have pro- Papua New Guinea (Georges et al., 2006; Rhodin and Genorupa,
vided for the first time, concrete evidence of a substantive decline 2000) are not connected to the local networks in the Kikori region.
in these pig-nosed turtle populations. We drew this conclusion An efficient transport infrastructure is absent in the Kikori region,
2286 C.C. Eisemberg et al. / Biological Conservation 144 (2011) 2282–2288

and the significant reduction in the body size of harvested female

turtles all point to the firm conclusion that the pig-nosed turtle had
suffered a substantial decline in population size in the past three
decades in the Kikori region.
Such a decline is unlikely to be restricted to the Kikori delta as
the species is under similar pressures elsewhere in PNG. In the Fly
River also, pig-nosed turtle eggs and meat provide an important
source of protein to complement agricultural produce (Georges
et al., 2006) and they are heavily harvested there (Rose et al.,
1982). Intensive egg harvest was also documented in the Purari
River (Pernetta and Burgin, 1980), and West Papua (Cann, 1978).
Around 1970, egg harvest increased substantially in the Eilanden
River (West Papua), when the region became more secure (Cann,
1998). Recently, it was estimated that 1.5–2 million eggs are annu-
ally harvested in the Merauke Regency (Samedi and Iskandar,
2000). In the Vriendschap River only adult turtles were usually
capture for consumption. However, egg collection has expanded
massively since 1997 due to the influx of eggs harvest from outside
West Papua (Maturbongs, 1999). Our data demonstrating a decline
in the Kikori gave indirect substance to claims of decline through-
out within its range in New Guinea and are likely to result in a re-
evaluation of the status of the species in New Guinea and globally.

4.1. Conservation Icon or Fishery?

Fig. 5. Comparison of the body size of nesting females of Carettochelys insculpta for
different nesting seasons of the Kikori. CCL, Maximum Curved Carapace Length in The global and local perspectives of the pig-nosed turtle are
cm. Means are given with 95% confidence limits (boxes) and ranges (vertical bars). dramatically different. There is a potential for tension during the
Nesting females were significantly smaller in 2007–2009 when compared with implementation of a conservation and management program for
1980–1981 (t = 2.53, df = 16.2, p < 0.05).
the pig-nosed turtle in the Kikori among indigenous people, wild-
life managers, researches and conservationists.
which can only be accessed by air or boat. Fuel is also a critical lim- Internationally, C. insculpta is a conservation icon. From the
iting factor for local villagers, which greatly limits any net returns. point of view of the local Papuan community, the pig-nosed turtle
Georges et al. (2008a) found no evidence of trade in turtles, eggs or is an important and traditional source of food, particularly protein,
turtle products with markets outside Kikori, only an anecdotal re- and a source of supplementary income through trade. A conserva-
port of live C. insculpta being shipped out of the region on logging tion ethic has yet to penetrate community perspectives, and many
boats for sale in the Asian market. However, we recorded crocodile villagers believe that the turtles are abundant, have always been
skin (Crocodylus novaeguineae and Crocodylus porosus) and numer- abundant and will continue to be so (Carla Eisemberg and Arthur
ous species of shark fin being actively collected for the interna- Georges, unpublished data). Those in the community who are con-
tional trade, which demonstrates the existence of a trade system cerned about the decline of the species are more concerned for sus-
that could potentially include turtles. tainability of the resource (for future generations) rather than as an
In this context, a shift from a subsistence economy to a cash endangered species issue in the western sense. The local villagers
economy and an accompanying shift toward reliance on processed view the species more as a fishery to be managed sustainably than
foods would be expected to reduce local demand for turtles. We as- a species to be conserved from the perspective of the international
sessed the impact of this possible confounding effect on our sur- conservation movement.
veys by a concurrent study of the impact of harvest on nest From a fishery management perspective, decline in abundance
survivorship. Our results showed an astonishing level of human is an inevitable consequence of exploitation, and is not of concern
harvest on eggs, which confirms an earlier unpublished report of unless and until the decline threatens sustainability of the re-
nest harvest rates of 85.6% (Pauza, 2003). Our results demonstrated source. Indeed, decline in a fishery stock ranging from 30% to
that, if there had been a reduction in harvest effort and hunting 60% (depending on the resilience of the species) in relation to its
acumen by local villagers as a result of the developing cash econ- virgin levels could be regarded as a normal and satisfactory out-
omy, it had not yet translated to a reduction in the outcome of come following the development of the fishery (Restrepo et al.,
the harvest – the rate remained exceptionally high. 1998). From a conservation perspective, any substantial decline
A third indication of the impact of harvest comes from the anal- in abundance of a globally restricted species such as the pig-nosed
ysis of turtle body size. Human harvest can alter demographic turtle is likely to trigger concern.
parameters of turtle populations (Close and Seigel, 1997; Fenberg So the two perspectives, indigenous and western, differ not in
and Roy, 2008; Fordham et al., 2007; Gamble and Simons, 2004; their common desire to see populations of the species persist in
Wolak et al., 2010). When a pristine population comes under har- perpetuity, but in their response to demonstrated decline in abun-
vest pressure, one of the first indicators is a reduction in body size dance and in the level at which the population can decline and still
(Bhupathy and Saravanan, 2006; Daza and Páez, 2007; Múnera be regarded as acceptable. This diversity in perspective is an
et al., 2004), both because the larger individuals are more likely important consideration in crafting a conservation plan for C. in-
to be targeted or retained and because of reduction in life expec- sculpta in PNG.
tancy, which in a species with indeterminate growth, translates
to a lower average body size in the population. We demonstrated 4.2. Achieving sustainability
a significant reduction in female body size in the past 30 years.
The combination of matched market and village surveys, the Programs to manage wildlife resources should be sustainable in
sustained and exceptionally high efficiency of human harvest, the long term, as well as biologically, economically and culturally
 C.C. Eisemberg et al. / Biological Conservation 144 (2011) 2282–2288 2287

acceptable (Bennett and Robinson, 2000; Campbell, 2002). Because M. Wa’abiya, S. Dekene, A. Nema, A. Moi, R. Kiapranis, M. Veao, S.
conservation is about sustaining values, and because the value of C. Ekali, K. Webb, (Oil Search), L. Kaia, D. Badi, F. Kinginapi (WWF)
insculta for the local population is centred on its use as food, not C. Alex and V. Kenisi (CDI), and J. Robins (NRI) assisted greatly with
the more esoteric concerns of the international community, a focus logistics. The Papua New Guinea Department of Environment and
on education to achieve sustainability of C. insculta as a fishery Conservation and L. Hill of the University of Papua New Guinea as-
would seem most appropriate. sisted us in gaining permission to undertake this research. This
There is a potential for utilizing C. insculpta under a sustainable project was funded by Oil Search, with in-kind support provided
yield management to provide a valuable protein source for local by the Worldwide Fund for Nature. M. Jensen, D. Bower, K. Hodges,
inhabitants (Rose et al., 1982). The central question here is D. Fielder and members of the Science Writers Workshop at the
whether it is possible to achieve sustainability given the combina- University of Canberra provided comments on drafts of this paper.
tion of life history attributes of the turtles (e.g. late maturing, slow-
growing, long-lived) and harvesting practices (focus on nesting fe-
References
males and eggs). Organisms with these life history attributes are
particularly susceptible to chronic disturbance and overexploita- Bennett, E.L., Robinson, J.G., 2000. Hunting of wildlife in tropical forests:
tion (Congdon et al., 1993), especially when large reproducing fe- implications for biodiversity and forest peoples. Environment Department
males are removed (Tucker and Moll, 1997). An extreme level of Papers, Biodiversity Series–Impact Studies, The World Bank Institute,
Washington, USA.
iteroparity (repeated reproduction) is required in species with Bhupathy, S., Saravanan, S., 2006. Status of marine turtles in the Gulf of Mannar,
low seasonal probability of reproductive success (Congdon et al., India. Chelonian Conservation and Biology 5, 139–141.
1993; Heppell, 1998). This concept promotes the perception that Bradshaw, C.J.A., Fukuda, Y., Letnic, M., Brook, B.W., 2006. Incorporating known
sources of uncertainty to determine precautionary harvests of saltwater
sustainable harvest of adult turtles is virtually impossible. How- crocodiles. Ecological Applications: A Publication of the Ecological Society of
ever, it has been demonstrated that long-lived reptiles can be sus- America 16, 1436–1448.
tainably harvested when appropriate management regimes are Broderick, A.C., Frauenstein, R., Glen, F., Hays, G.C., Jackson, A.L., Pelembe, T., Ruxton,
G.D., Godley, B.J., 2006. Are green turtles globally endangered? Global Ecology
implemented both for crocodiles (Bradshaw et al., 2006) and tur- and Biogeography 15, 21–26.
tles (Fordham et al., 2007). Nevertheless, it is not known where Browne, C.L., Hecnar, S.J., 2007. Species loss and shifting population structure of
C. insculpta is situated in the ‘slow-fast’ (recruitment, growth, freshwater turtles despite habitat protection. Biological Conservation 138, 421–
429.
maturity) continuum of life history characteristics and the ques- Busse, M., Turner, S., Araho, N., 1993. The people of Lake Kutubu and Kikori:
tion as to whether any level of harvest in the Kikori region is sus- changing meanings of daily life. Papua New Guinea National Museum, Port
tainable remains open. Moresby, Papua New Guinea.
Campbell, L.M., 1998. Use them or lose them? Conservation and the consumptive
Although a definitive answer to this question is not known, we
use of marine turtle eggs at Ostional, Costa Rica. Environmental Conservation
do know that reptiles, especially turtle eggs and meat, are an 25, 305–319.
important and seasonal source of protein for many rural popula- Campbell, L.M., 2002. Science and sustainable use: views of marine turtle
tions in developing countries, and a potential source of supplemen- conservation experts. Ecological Applications 12, 1229–1246.
Cann, J., 1978. Tortoises of Australia. Angus and Robertson, Sydney, Australia.
tary income through trade (Klemens and Thorbjarnarson, 1995; Cann, J., 1998. Australian Freshwater Turtles. Beaumont Publishing, Singapore.
Mittermeier et al., 1992). Complete elimination of pig-nosed turtle Close, L.M., Seigel, R.A., 1997. Differences in body size among populations of red-
harvest in Kikori could potentially aggravate their already protein- eared sliders (Trachemys scripta elegans) subjected to different levels of
harvesting. Chelonian Conservation and Biology 2, 563–566.
deficient diet (Foley, 1986). Exclusionary and restrictive conserva- Congdon, J.D., Dunham, A.E., Sels, R.C.V.L., 1993. Delayed sexual maturity and
tion practices in developing countries have often alienated local demographics of blanding’s Turtles (Emydoidea blandingii): implications for
people and failed to protect the wildlife (Pimbert and Pretty, conservation and management of long-lived organisms. Conservation Biology 7,
826–833.
1998). It is unlikely that any efforts to dramatically curtail the har- Connell, J., 1997. Papua New Guinea: The Struggle for Development. Routledge, New
vest of pig-nosed turtles would be acceptable to the local commu- York, USA.
nity and any attempt to do so could lead to counterproductive David, B., 2008. Rethinking cultural chronologies and past landscape engagement in
the Kopi region, Gulf Province, Papua New Guinea. The Holocene 18, 463–479.
attitudes to conservation on broader agendas. Daza, J.M., Páez, V.P., 2007. Morphometric variation and its effect on reproductive
Our study in the Kikori region is likely representative of harvest potential in female Colombian slider turtles (Trachemys callirostris callirostris).
regimes in most areas within the species range in PNG, from the Herpetologica 63, 25–134.
Dudgeon, D., Arthington, A.H., Gessner, M.O., Kawabata, Z.-I., Knowler, D.J., Lévêque,
Purari River in the east to the Fly River in the west, and provides
C., Naiman, R.J., Prieur-Richard, A.-H., Soto, D., Stiassny, M.L.J., Sullivan, C.A.,
lessons for conservation of many other wildlife subject to harvest. 2006. Freshwater biodiversity: importance, threats, status and conservation
This type of scenario calls for a holistic approach that integrates all challenges. Biological Reviews of the Cambridge Philosophical Society 81, 163–
biological, socioeconomic and political disciplines (Campbell, 182.
Enesar Consulting, 2005. Environmental impact statement. PNG Gas Project, In
1998; Frazer, 1992; Ludwig, 1993; Marcovaldi and Marcovaldi, Report CR 790_20_Rev4. Esso Highlands, Port Moresby, Papua New Guinea.
1999; Milner-Gulland and Bennett, 2003). The approach needs to Fenberg, P.B., Roy, K., 2008. Ecological and evolutionary consequences of size-
be adaptive, where communities continue to draw upon the re- selective harvesting: how much do we know? Molecular Ecology 17, 209–220.
Foley, W.A., 1986. The Papuan languages of New Guinea. Cambridge University
source concurrent with monitoring that is sufficiently robust to Press, Cambridge, UK.
quantify trends in abundance. Without community-led action in- Fordham, D.A., Georges, A., Brook, B.W., 2007. Demographic response of snake-
formed by applied research and environmental education, sup- necked turtles correlates with indigenous harvest and feral pig predation in
tropical northern Australia. Journal of Animal Ecology 76, 1231–1243.
ported by wildlife protection, and adequately funded by those Fordham, D.A., Georges, A., Brook, B., 2009. Experimental evidence for density
industries gaining most from natural resource development, the dependent responses to mortality of snake-necked turtles. Oecologia 159, 271–
current declines may continue to yield unsatisfactory outcomes 281.
Frazer, N.B., 1992. Sea turtle conservation and halfway technology. Conservation
from both fishery and conservation perspectives. Biology 6, 179–184.
Gamble, T., Simons, A.M., 2004. Comparison of harvested and nonharvested painted
Acknowledgments turtle populations. Wildlife Society Bulletin 32, 1269–1277.
Georges, A., Guarino, F., Bito, B., 2006. Freshwater turtles of the TransFly region of
Papua New Guinea: notes on diversity, distribution, reproduction, harvest and
We would like to thank the many people who assisted us in the trade. Wildlife Research 33, 373–384.
field, but especially our translators M. Boru and B. Oni and our vol- Georges, A., Doody, S., Eisemberg, C., Alacs, E., 2008a. Carettochelys insculpta
unteer field assistants L. Bauer, R.F. Silva and S. Reynolds for their Ramsay 1886–Pig-Nosed Turtle, Fly River Turtle. Chelonian Research
Monographs 1, 17.
exceptional efforts and companionship. We are grateful to all the Georges, A., Alacs, E., Pauza, M., Kinginapi, F., Ona, A., Eisemberg, C., 2008b.
villages we visited for sharing their knowledge with us. J. Kaiwari, Freshwater turtles of the Kikori Drainage, Papua New Guinea, with special
2288 C.C. Eisemberg et al. / Biological Conservation 144 (2011) 2282–2288

reference to the pig-nosed turtle, Carettochelys insculpta. Wildlife Research 35, Guidance on the Use of Precautionary Approaches to Implementing National
700–711. Standard 1 of the Magnuson-Stevens Fishery Conservation and Management
Groombridge, B., Wright, L., 1982. The IUCN Amphibia-Reptilia red data book. Part Act. In: NOAA Technical Memorandum NMFS-F/SPO-31. Washigton, USA.
1, Testudines, Crocodylia, Rhynchocephalia. IUCN, London, UK. Rhodin, A.G.J., Genorupa, V.R., 2000. Conservation status of freshwater turtles in
Heppell, S.S., 1998. Application of life-history theory and population model analysis Papua New Guinea. Chelonian Research Monographs 2, 129–136.
to turtle conservation. Copeia 1998, 367–375. Rhodin, A.G.J., Walde, A.D., Horne, B.D., van Dijk, P.P., Blanck, T., and Hudson, R.,
Humber, F., Godley, B.J., Ramahery, V., Broderick, A.C., 2010. Using community 2011. Turtles in Trouble: The World’s 25+ Most Endangered Tortoises and
members to asses artisanal fisheries: the marine turtle fishery in Mandagascar. Freshwater Turtles—2011. IUCN/SSC Tortoise and Freshwater Turtle Specialist
Animal Conservation 14, 175–185. Group, Turtle Conservation Fund, Turtle Survival Alliance, Turtle Conservancy,
IUCN, 2009. IUCN Red list of Threatened Species. Version 2009.2. Chelonian Research Foundation, Conservation International, Wildlife
<www.iucnredlist.org> (accessed August 2010). Conservation Society, and San Diego Zoo Global, Lunenburg, Canada.
Klemens, M.W., Thorbjarnarson, J.B., 1995. Reptiles as a food resource. Biodiversity Romero, A., Baker, R., Creswell, J.E., 2002. Environmental History of marine mammal
and Conservation 4, 281–298. exploitation in Trinidad and Tobago, W.I., and its ecologica impact.
Laurance, W.F., Cochrane, M.A., Bergen, S., Fearnside, P.M., Delamônica, P., Barber, C., Environment and History 8, 255–274.
D’Angelo, S., Fernandes, T., 2001. Environment: the future of the Brazilian Rose, M., Parker, F., Rhodin, A.G.J., 1982. New Guinea plateless turtle or pitted shell
Amazon. Science 291, 438–439. turtle (Fly River or pig-nosed turtle), Carettochelys insculpta Ramsay 1886. In:
Löffler, E., 1977. Geomorphology of Papua New Guinea. Australian National Groombridge, B., Wright, L. (Eds.), The IUCN Amphibia-Reptilia Red Data Book,
University Press, Canberra, Australia. Part 1, Testudines, Crocodylia and Rhychocephalia. IUCN, London, UK, pp. 243–
Low, B., Sundaresan, S.R., Fischhoff, I.R., Rubenstein, D.I., 2009. Partnering with local 246.
communities to identify conservation priorities for endangered Grevy’s zebra. Rosser, A.M., Mainka, S.A., 2002. Overexploitation and species extinctions.
Biological Conservation 142, 1548–1555. Conservation Biology 16, 584–586.
Ludwig, D., 1993. Environmental sustainability: magic, science, and religion in Salas, S., Chuenpagdee, R., Seijo, J.C., Charles, A., 2007. Challenges in the assessment
natural resource management. Ecological Applications 3, 555–558. and management of small-scale fisheries in Latin America and the Caribbean.
Marcovaldi, M.Â., Marcovaldi, G.G., 1999. Marine turtles of Brazil: the history and Fisheries Research 87, 5–16.
structure of Projeto TAMAR-IBAMA. Biological Conservation 91, 35–41. Samedi, M.L., Iskandar, D.T., 2000. Freshwater turtle and tortoise conservation and
Marsh, H., Lawlerm, I.R., Kwan, D., Delean, S., Pollock, K., Alldredge, M., 2004. Aerial utilization in Indonesia. Chelonian Research Monographs 2, 106–111.
surveys and the potential biological removal technique indicate that the Torres Samedi, A.R., Iskandar, D.T., 2002. Utilization and trade in freshwater turtles and
Strait dugong fishery is unsustainable. Animal Conservation 7, 435–443. tortoises in Indonesia. In: C.R. Fundation, (Ed.), Technical Workshop on
Maturbongs, J.A., 1999. Trade monitoring of pig nose turtle (Carettochelys insculpta) Conservation of and Trade in Freshwater Turtles and Tortortoises in Asia,
from Vriendschap River, District of Suator, Merauke Regency, Irian Jaya. In: Kunming, Yannan Province, Peoples Republic of China, pp. 25–28.
Noerdjito, N., Maryanto, I. (Eds.), Jenis-jenis hayati yang dilindungi Shepherd, C.R., Nijman, V., 2007. An overview of the regulation of the freshwater
perundangundangan Indonesi. Lembaga Ilmu Pengetahuan Indonesia (LIPI) turtle and tortoise pet trade in Jakarta, Indonesia. TRAFFIC Southeast Asia, Kuala
and The Nature Conservancy, Cibinong, Indonesia, pp. 21–27. Lumpur, Malaysia.
Milner-Gulland, E.J., Bennett, E.L., 2003. Wild meat: the bigger picture. Trends in Smith, N.J.H., 1979. Aquatic turtles of Amazonia: an endangered resource. Biological
Ecology & Evolution 18, 351–357. Conservation 16, 165–179.
Mittermeier, R.A., Carr, J.L., Swingland, I.R., Werner, T.B., Mast, R.B., 1992. Sodhi, N.S., Koh, L.P., Brook, B.W., Ng, P.K.L., 2004. Southeast asian biodiversity: an
Conservation of amphibians and reptiles. In: Adler, K. (Ed.), Herpetology: impending disaster. Trends in Ecology & Evolution 19, 654–660.
Current Research on the Biology of Amphibians and Reptiles. Society for the Sokal, R.R., Rohlf, F.J., 1981. Biometry. The principles and practice of statistics in
Study of Amphibians and Reptiles, Oxford, OH, pp. 59–80. biological research. WH Freeman, New York, USA.
Mittermeier, R.A., Mittermeier, C.G., Gil, P.R., 1997. Megadiversity: Earth’s Spotila, J.R., Reina, R.D., Steyermark, A.C., Plotkin, P.T., Paladino, F.V., 2000. Pacific
Biologically Wealthiest Nations. Cemex, Monterrey, Mexico. leatherback turtles face extinction. Fisheries can help avert the alarming decline
Múnera, M.B., Daza, J.M., Páez, V.P., 2004. Ecología reproductiva y cacería de la in population of these ancient reptiles. Nature 405, 529–530.
tortuga Trachemys scripta (Testudinata: Emydidae), en el área de la Depresión Soykan, C.U., Moore, J.E., Zydelis, R., Crowder, L.B., Safina, C., Lewison, R.L., 2008.
Momposina, norte de Colombia. Revista de Biología Tropical 52, 229–238. Why study by catch? An introduction to the theme section on fisheries by catch.
Musick, J.A., 1999. Ecology and conservation of long-lived marine animals. Endangered Species Research 5, 91–102.
American Fisheries Society Symposium 23, 1–10. Townsend, W.R., Randall Borman, A., Yiyoguaje, E., Mendua, L., 2005. Cofán indians’
Pauza, M., 2003. The pig-nosed turtle project. Report to the World Wide Fund for monitoring of freshwater turtles in Zábalo, Ecuador. Biodiversity and
Nature Boroko, Papua New Guinea. Conservation 14, 2743–2755.
Pernetta, J.C., Burgin, S., 1980. Census of crocodile populations and their Tucker, J.K., Moll, D., 1997. Growth, reproduction, and survivorship in the red-eared
exploitation in the Purari area (with an annotated checklist of the turtle, Trachemys scripta elegans. Chelonian Conservation and Biology 2, 352–
herpetofauna). Purari River (Wabo) Hydroelectric Scheme Environmental 357.
Study 14, 1–44. van Dijk, P.P., Iskandar, D.T., Palasuwan, T., 2000. Turtle trade in southeast asia:
Pimbert, M.P., Pretty, J.N., 1998. Diversity and sustainability in community based regional summary (Indonesia, Malaysia, Papua New Guinea, and Thailand).
conservation. In: Kothari, A., Pathak, N., Anuradha, R.V., Taneja, B. (Eds.), Chelonian Research Monographs 2, 145–147.
Communities and Conservation: Natural Resource Management in South and Wolak, M.E., Gilchrist, G.W., Ruzicka, V.A., Nally, D.M., Chambers, R.M., 2010. A
Central Asia. Sage Publications, New Delhi, India, pp. 58–77. contemporary, sex-limited change in body size of an estuarine turtle in
Restrepo, V.R., Thompson, G.G., Mace, P.M., Gabriel, W.L., Low, L.L., MacCall, A.D., response to commercial fishing. Conservation Biology 24, 1268–1277.
Methot, R.D., Powers, J.E., Taylor, B.L., Wade, P.R., Witzig, J.F., 1998. Technical