Biological Conservation 116 (2004) 35–47
www.elsevier.com/locate/biocon
The conservation status of Townsend’s shearwater
Puffinus auricularis auricularis
Juan E. Martı́nez-Gómeza,*, Jeff K. Jacobsenb
a
Department of Biology, Villanova University, Villanova, PA 19085, USA
Department of Biological Sciences, Humboldt State University, Arcata, CA 95521, USA
b
Received 8 March 2002; received in revised form 18 March 2003; accepted 20 March 2003
Abstract
Townsend’s shearwater (Puffinus auricularis auricularis) is an endangered seabird endemic to the Revillagigedo Archipelago. It
nested on Socorro, Clarion, and San Benedicto Islands. It was extirpated by the Barcena volcano on San Benedicto in 1952, and
there are no recent indications of nesting. Introduced mammals—pigs and rabbits—preyed on them and destroyed habitat at
Clarion; shearwaters were extirpated by 1988, and no breeding attempts have been reported since. Our results confirm that Socorro
holds the last breeding grounds. We found breeding colonies above 800 m and a minimum population of 1100 individuals. This
represents a significant reduction in distribution and population size. Intensive cat predation at Socorro could potentially kill ca.
350 females per season, and sheep progressively destroy nesting areas. Population projections suggest that demographic instability
could occur in less than 100 years under severe predation and habitat degradation. Only low predation rates would allow population persistence for more than 150 years in spite of a declining population. Thus, the immediate eradication of all introduced
mammals is necessary to prevent the extinction of this seabird.
# 2003 Elsevier Ltd. All rights reserved.
Keywords: Townsend’s shearwater; Puffinus auricularis; Revillagigedo Archipelago; Socorro Island; Matrix models
1. Introduction
Townsend’s shearwater (Puffinus auricularis auricularis; AOU, 1998) is an endangered seabird endemic
to the Revillagigedo Archipelago (Ainley et al., 1997).
Three of the four islands in that region were suitable for
nesting by Townsend’s shearwater: Socorro, Clarion,
and San Benedicto. These islands are among the least
impacted in the Pacific, because limited human colonization began only recently and damage caused by
introduced animals can be reversed almost entirely. The
archipelago is noteworthy for its high levels of endemism in flora and fauna (Levin and Moran, 1989;
Brattstrom, 1990).
Townsend’s shearwater was first discovered at Clarion
in 1889 (Townsend, 1890). Subsequently, breeding
grounds were detected there and at San Benedicto in 1897
(Anthony, 1898), and at Socorro in 1925 (McLellan,
* Corresponding author. Present address: Department of Biology,
University of Missouri—St. Louis, St. Louis, MO 63121, USA.
E-mail address: mimodes@jinx.umsl.edu (J.E. Martı́nez-Gómez).
0006-3207/03/$ - see front matter # 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0006-3207(03)00171-X
1926). The colonies at San Benedicto were destroyed by
the eruption of the Barcena volcano in 1952 (Brattstrom
and Howell, 1956), and introduced mammals extirpated
those at Clarion by the late 1980s (Everett, 1988; Howell
and Webb, 1989). Thus, it would seem that the last
remaining breeding grounds for this subspecies are on
Socorro.
Although Townsend’s shearwater is considered at
risk, lack of information has made it impossible to
determine its precise status (Collar et al., 1992). Some
authors have considered this shearwater to be the most
endangered seabird of the offshore islands of the Mexican Pacific (Everett and Anderson, 1991). Mounting
evidence suggests that it is critically endangered (BirdLife, 2000).
Population size has not been assessed adequately, but
there are reports ranging from several hundred to several thousand birds. Jehl (1982) estimated a Socorro
population of at least 1000 breeding pairs by counting
birds returning to land. Spear et al. (1995) used at-sea
density data from 15 years (early 1980s–mid 1990s) of
surveys to estimate total pelagic populations of 46,400
36
J.E. Martı´nez-Gómez, J.K. Jacobsen / Biological Conservation 116 (2004) 35–47
individuals, of which 10,600 were breeding pairs. During the breeding season, individuals in reproductive
condition are at Socorro, but most non-breeding individuals are found in the Middle American Trench offshore Mexico’s Pacific coast from Jalisco to Guerrero
(Howell and Engel, 1993).
Habitat destruction and predation caused by introduced mammals are the most serious threats to
Townsend’s shearwater. On Clarion, breeding colonies
were destroyed by the late 1980s. In January 1986, only
unoccupied burrows were observed (Everett, 1988). In
February 1988, the damage to nesting areas caused by
introduced pigs and rabbits was extensive and shearwater carcasses were observed frequently on the ground
(Howell and Webb, 1989).
On Socorro, the impact of cat predation has been
contested. Jehl and Parkes (1982) suggested that cat
predation was an imminent threat after observing several shearwater carcasses, presumably killed by cats.
Rodrı́guez-Estrella et al. (1991) and Wehtje et al. (1993)
did not agree with that assessment because they failed to
find cat sign in the shearwater’s breeding areas. More
recently, Martı́nez-Gómez and Curry (1995; 1996)
found shearwater remains in cat scats and stomach
contents, as well as carcasses eaten in a way indicative
of cat predation (c.f. Veitch, 1985). Such observations
confirm that cats pose a serious threat to this species.
In this paper, we provide an assessment of the current
status of Townsend’s shearwater as well as information
about its population size and distribution. We focused
our efforts on the extant breeding colony at Socorro,
but surveyed Clarion to determine if shearwaters had
returned. The effect of habitat destruction, cat predation, and demographic stochasticity on this endangered
subspecies was evaluated using matrix population projections. By combining information on population size
and estimated levels of habitat loss and predation, we
were able to estimate the time frame in which Townsend’s shearwater may reach demographic instability.
We also discuss several conservation steps necessary to
avert this species’ extinction.
1987, 1 February–7 March 1988, 15 January–7 March
1989, 18 January–18 April 1991, 5 March–4 April 1995,
18 January–4 April 1996, 18 January–18 April 1997, 18
January–18 April 1998, 18 January–18 April 1999, 4
February–18 April 2000, and Clarion on 5 April 1995,
19 January 1996, 9–14 April 1997, 4–18 March 1998, 5
February–6 April 1999, 5 February–6 April 2000. Most
data were gathered during 1993–1997.
2.1. Distribution and population size
Socorro and Clarion were surveyed to estimate
shearwater numbers and determine the extent of current
breeding areas. On Socorro, 40 campsites served as
nocturnal sampling stations (Fig. 1). Nine were located
below 500 m, and 31 above 500 m around Mount
Evermann. Most of these sites were placed in five different regions around Mount Evermann (north, northwest, east and west forests, and the central plateau). A
coarse estimate of breeding population size was
obtained by summing the maximum count of birds
returning to each of the five regions throughout our
study. Birds were detected visually or by listening to
their calls during moonless nights. We did not count
birds at their burrows because of the risk of facilitating
cat predation. Our population estimate was compared
with that of Spear et al. (1995) to help us choose a realistic initial population vector for matrix projections. On
Clarion, the entire island was surveyed, but especially
those areas where shearwaters had been previously
reported (Fig. 2; Everett, 1988; Howell and Webb, 1989)
and areas with suitable habitat. A night station was
established near the military garrison to listen for
incoming shearwaters.
We also searched for shearwaters resting or flying at sea
during daily near-shore (5 km) surveys around Socorro
and Clarion. We looked carefully for shearwaters flying
offshore of Clarion as these birds could be prospecting for
burrows or attempting to breed. In addition, marine surveys were conducted from naval transport vessels while
approaching or departing these two islands.
2.2. Predation
2. Methods
Opportunistic terrestrial and maritime samplings were
conducted on Socorro and Clarion at different periods
during 1986–2000 while conducting studies on Socorro
Mockingbirds (Mimodes graysoni; JEMG) and Humpback whales (Megaptera novaeangliae; JKJ). JEMG visited Socorro from 20 May to 5 June 1988, 6–19 January
and 6 June–5 August 1993, 18 February–4 June 1994, 20
March–19 May 1995, 20 January–3 April 1996, and 19
June–10 August 1997, and Clarion on 6 June 1988, 19
March 1995, and 19 January 1996. JKJ visited Socorro
on 15 January–21 February 1986, 15 January–7 March
On Socorro, we searched for cat sign in multiple areas
of the island (Fig. 1). Trails to the different sampling
stations were used as sampling transects, and cat scats
were collected every 4–6 days. Cats were trapped with
leg-hold, Tomahawk, and Havahart traps. Additionally,
military personnel hunted cats with firearms. Scats and
stomach contents were examined to determine cat diet.
Bird remains were identified from feathers, beaks, bones
and/or claws; mouse and lizard remains from bones,
fur, skin and/or scales; and invertebrate remains by
their shape and texture. Our sampling scheme allowed
us to obtain an idea of cat distribution and diet, but it
J.E. Martı´nez-Gómez, J.K. Jacobsen / Biological Conservation 116 (2004) 35–47
37
Fig 1. Map showing the locations of trails used to gather cat sign and the location of 40 nocturnal sampling stations. Squares with dots show those
stations where shearwaters were observed landing.
was not designed to obtain a population estimate. In
addition to cats, Socorro red-tailed hawks (Buteo
jamaicensis socorroensis) are a natural predator of
Townsend’s shearwater (Martı́nez-Gómez and Curry,
1995). We assessed qualitatively predation by red-tailed
hawks by inspecting nest contents and by searching
under hawk perches for shearwater remains.
Previously published information on cat distribution
and diet (Martı́nez-Gómez and Curry, 1996) is supplemented with subsequent findings. We estimated the number of shearwaters (s) killed per cat per breeding season
using the proportion (p) of cat scats that had shearwater
remains following the methods of Apps (1983):
s ¼ ðpÞðdÞ r1 ðkÞðbÞ
of an ‘‘average’’ cat. We assumed that cats defecate one
scat per day (d=1), that shearwater remains in a scat
came from a single bird (r=1) and that cats killed 90%
(k=0.9) of the shearwaters while the other 10% was
scavenged from birds killed by hawks. We also assumed
a shearwater breeding season of 8 months (b=240
days). Thus, the total number of female shearwaters (T)
killed by cats during the breeding season would vary
proportionally to the size (N) of the predator population [T=(s/2)(N)]. Although these estimates might not
be accurate in the presence of a prey-specialist predator,
they are still helpful in evaluating the impact of different
hypothetical predation levels.
Thus, if all cats have similar prey preferences, the
proportions of the different prey items represent the diet
Matrix models have been used as a heuristic tool to
evaluate the contribution of different factors to the
2.3. Population projections
38
J.E. Martı´nez-Gómez, J.K. Jacobsen / Biological Conservation 116 (2004) 35–47
Fig. 2. Previously reported locations of Townsend’s Shearwater breeding grounds at Isla Clarion. Of these, two were found on hilltops and two in a
central plateau between two hills.
demography of endangered species (Caswell, 2001). The
impact of cat predation and/or various anthropogenic
factors on the populations of Newell’s (Puffinus a. newelli) and black-vented (P. opisthomelas) shearwaters has
been explored using deterministic matrix models (Ainley
et al., 2001; Keith et al., 2002). Encouraged by the versatility of these models, we estimated a possible time
frame in which Townsend’s shearwater may reach
demographic instability by projecting the change of a
hypothetical population affected by habitat degradation, cat predation and demographic stochasticity. Only
females and their daughters are considered in our projections; thus, all demographic parameters are adjusted
accordingly. We explored six possible scenarios: (1) the
fate of a slow growing population, (2) the impact of
severe habitat degradation, (3) low and (4) high predation scenarios and severe habitat degradation combined
with (5) low and (6) high predation. For each model, we
determined the finite rate of increase (l), the annual rate
of decrease, population size at t=150, time to extinction
(arbitrarily set as the point where population size
becomes less than 2), and the time in which the last 100
females occur. Matrix analyses and projections were
carried out using PopTools 2.5.3 for Windows (http://
www.cse.csiro.au/poptools); projection files are available from the authors upon request.
3. Life cycle reconstruction
Prior to demographic modeling, a reliable reconstruction of this species’ life cycle is required. The
breeding biology for this seabird can be reconstructed
from the reports of expeditions to the archipelago in
1897 (Anthony, 1898, 1900; Kaeding, 1905) and 1925
(Hanna, 1926; McLellan, 1926). Young as large as
adults (half grown, 35 days old if growth patterns are
similar to those of Manx shearwater; Brooke 1990) and
one egg in advanced incubation ( 50 days if it was
about to hatch) were reported on San Benedicto and
Clarion by both parties during 30 April–1 May. Wellgrown young (perhaps 60–70 days old) were reported
during 20–27 May on Clarion (Anthony, 1898; Kaeding, 1905). However, only young in pteroptyle down
from both islands were archived in museum collections.
Those specimens could not be older than 2 weeks considering their wing chords (1 May: USNM 162003=29
mm, CAS 28164=25 mm, CAS 28165=36 mm; 25
May: USNM 162004=41 mm).
Thus, it appears that birds begin gathering at the
islands by mid-November to prospect for burrows; a
pre-laying period of one or two months should follow
(Jehl, 1982). They should begin laying from late January to mid-March and fledging young from late May
to mid-July as previously conjectured (Jehl, 1982), with
little to no fledging occurring after. Ainley et al. (2001)
suggested that the islands in the archipelago might
have a different laying phenology based on a report of
very small young on San Benedicto by late May
(Anthony, 1900). However, closer inspection of that
account suggests a printing error because the other
reports of the 1897 expedition only mention young on
that island by late April (Anthony, 1898; Kaeding,
1905).
J.E. Martı´nez-Gómez, J.K. Jacobsen / Biological Conservation 116 (2004) 35–47
It is also conceivable that if Townsend’s shearwater
has a similar life history to that of Newell’s shearwater
(e.g. Ainley et al., 1997), young birds would not return
to the breeding grounds, subadults would return after
adults have finished laying their eggs, and pair bonding
would begin during the fourth and fifth years. Most
birds would begin breeding by ages 5 or 6, if age of first
reproduction parallels that of the Manx shearwater (e.g.
Brooke, 1990).
4. Stable population
The fate of a stable population was studied by
assembling a matrix using demographic parameters
from similar sized shearwaters. We followed the criteria
for a post-breeding census (e.g. McDonald and Caswell,
1993; Caswell, 2001); therefore, the first survival rate
(P21) represents the transition from fledglings to 1-yearold birds (that probability would be incorporated into
fertility values under a pre-breeding census). Survival
rates (Pij) increased with age; for the first three years of
life they were 0.654, 0.780, 0.890, and 0.905 thereafter
(e.g. Perrins et al., 1973; Ainley et al., 2001). Our matrix
has two fertility values (F15, F16); these values were
modeled as the product of adult survival rates, breeding
probability and breeding success of first-time and
experienced breeders. We used breeding success values
from an undisturbed colony of the Manx shearwater;
females in their first breeding year produce fewer female
chicks than experienced females. Breeding probability
was adjusted to produce a finite rate of increase (l)
slightly greater than one; such a value represents the
minimum proportion of breeding females required to
maintain a stable population. In doing so, our model
resembles the small growth rates observed in other
pelagic birds (Russell, 1999).
Our work on Socorro Island prompted us to begin
our projections using the worst-case demographic scenario suggested for this seabird (Spear et al., 1995).
Thus, our initial population vector consisted of a total
of 8750 females of which 2625 (30%) were sexually
mature; the remaining birds were distributed evenly
among classes 1–5 (1225 per class). Population projections were run for 150 years. Average population trajectories and 95% confidence intervals for these
projections were obtained through Monte Carlo simulations incorporating demographic stochasticity; we ran
10,000 simulations for each projected matrix. We
allowed the number of survivors at time t+1 to be a
binomial random number based on the survival rate and
number of individuals in the previous age class at time t.
Fertility components varied according to published
deviation estimates for similar sized shearwaters. Matrix
parameters for this and subsequent models are shown in
Table 1.
39
5. Habitat degradation
Presumably, habitat degradation and loss could
impact demographic parameters of a life cycle in various manners. In the absence of data, most parameters
were left the same as in a stable population, but breeding probability was reduced to model the loss of nesting
burrows. We derived a value for breeding probability
from our colony-based census on Socorro and the
number of mature females in the initial population vector. We assumed that habitat destruction proceeds at a
rate that maintains breeding probability constant
despite a declining population. Confidence intervals
were obtained through Monte Carlo simulations.
6. Cat predation
The impact of cat predation was estimated by recalculating survival rates and fertility values of age classes
affected by predation. The number of survivors under
low and high predation scenarios results from subtracting the number of female shearwaters taken by 1 or 10
‘‘average’’ cats (sensu Apps, 1983) and those dying of
natural causes from the initial population vector. We
assumed that only the three oldest age classes were
taken by cats. The total number of killed shearwaters
represents the sum of all deaths happening during the
entire breeding season. Our model takes into consideration the fact that predation of birds 4–5 years old occurs
predominantly in the first months of the breeding season, whereas that of birds 6 years old or older happens
at the end. For practical purposes, we considered predation on nestlings to be nil because they remain in their
burrows until fledging; upon departure to the sea they
will not return to the breeding grounds until they reach
sexual maturity.
Thus, the number of 6-year-old females or older eaten
by cats was determined by multiplying the estimated
total number of breeding females killed under low and
high predation scenarios by the proportion of that age
class in the stable age distribution of the stable population. The remaining number of killed females was divided equally between ages four and five. Although
arbitrary, this assignation describes a plausible pattern
of mortality where mature females would suffer the
greatest impact due to their longer stay on the island
(but see Ainley et al., 2001; Keith et al., 2002).
After the impact of predation was incorporated, survival rates in the age classes affected by predation varied
randomly following a normal distribution with an average and standard deviation determined from annual
variation in scat contents (Table 1). Then, we estimated
the number of survivors in affected age classes as a
binomial random number as in previous models. By
keeping average survival rates constant, we assumed
40
J.E. Martı´nez-Gómez, J.K. Jacobsen / Biological Conservation 116 (2004) 35–47
Table 1
Demographic parameters used in population projections refer to females in the populationa
Non-zero matrix elements
Stable
population
Habitat
degradation
(HD)
Low
predation
(LP)
High
predation
(HP)
HD & LP
HD & HP
Variation
around
parameter
Initial
population
vector
F15
F16
P21
P32
P43
P54
P65
P66
Fertility components
Breeding Probability 5th Age Class
Breeding Probability 6th Age Class
Breeding Success 5th Age Class
Breeding Success 6th Age Class
0.193777
0.240314
0.654
0.780
0.890
0.905
0.905
0.905
0.059843
0.074215
0.654
0.780
0.890
0.905
0.905
0.905
0.190951
0.236454
0.654
0.780
0.890
0.898595
0.898595
0.89736
0.178701
0.218336
0.654
0.780
0.890
0.840945
0.840945
0.828601
0.058970
0.073023
0.654
0.780
0.890
0.898595
0.898595
0.897360
0.055187
0.067427
0.654
0.780
0.890
0.840945
0.840945
0.828601
b
0.011741c
0.011741c
0.014004c
–
–
1225
1225
1225
1225
1225
2625
0.68
0.68
0.31488
0.3905
0.21
0.21
0.31488
0.3905
0.68
0.68
0.31488
0.3905
0.68
0.68
0.31488
0.3905
0.21
0.21
0.31488
0.3905
0.21
0.21
0.31488
0.3905
0.07054d
0.059235d
0.07054
0.059235
–
–
–
–
b
c
c
c
a
Survival rates for the stable population come from Ainley et al. (2001). Fertility values are the product of survival rates from the 5th and 6th age
classes, breeding success (Brooke, 1990), and breeding probability (adjusted to obtain a stable population). Fertility values and survival rates were
adjusted further to incorporate habitat degradation and predation. The initial population vector corresponds to the worst demographic scenario
suggested by Spear et al. (1995).
b
Variation around fertility values resulted from the variation in its three components.
c
Variation in survival rates followed a binomial distribution. Survival rates for the last three age classes first varied according to differences in
prey proportions observed in scats; then as a binomial variate.
d
Variation around breeding probabilities was arbitrarily set equal to that of breeding success (from Brooke, 1990) for the same age class.
that cats inflict the same proportional impact as the
population declines. This assumption might not hold in
the presence of prey-specific predators or if densitydependent factors occur. Confidence intervals for the
remaining parameters were established as before.
7. Habitat degradation and cat predation
The combined effect of these two risk factors was
evaluated by incorporating the impact of habitat degradation into the two previous predation models. This
exercise allows one to evaluate the relative impact of
each threatening factor and to identify those age classes
that require protection when habitat loss and predation
act concurrently.
8. Results
8.1. Distribution and population size
Our surveys confirmed that Socorro holds the last
breeding colonies of Townsend’s shearwater. At Clarion, our only marine detection was of five shearwaters
37 km east of the island on 19 January 1996 while in
transit in a navy vessel. No shearwaters were seen in the
vicinity of Clarion during daily offshore surveys during
1997–2000. On Socorro, shearwaters were found frequently in groups ranging from 3 to 10 individuals and
less frequently in groups > 50 individuals. We saw >
100 shearwaters resting on the waters 23 km west of
Socorro on 13 January 1996 and > 20 foraging individuals 35 km southwest of the island on 20 January 1996.
These results suggest that most shearwaters are found at
Socorro.
Terrestrial surveys corroborated that pattern. At
Clarion Island in 1998–2000, no active burrows were
detected. The areas where shearwaters had previously
been observed nesting (Fig. 2) no longer had suitable
habitat and were infested by rabbits. On Socorro,
breeding areas were found on Mount Evermann in
dense shrubs and forests above 800 m (Fig. 1). Colonies
apparently remained active until mid-summer. We
detected shearwaters coming to land during June and
July 1993 and 1997. However, during the same months
in 1997, we detected only a few individuals returning to
montane areas at night. We also found fledglings landing on the Naval Base in June 1993, perhaps attracted
by streetlights. Our findings suggest that the breeding
phenology of Townsend’s shearwaters coincides with
our reconstruction and that breeding colonies are not
active beyond July. However, both of these years were
influenced by the El Niño Southern Oscillation (ENSO)
and perhaps are not representative of other years.
Breeding and roosting areas of Townsend’s shearwater coincide with the core set of territories of Socorro
Mockingbirds around Mount Evermann. This area
covers about 6 km2 and represents < 10% of the island’s
surface (Martı́nez-Gómez and Curry, 1996). The dominant trees are Ilex socorroensis and Guettarda insularis,
while Triumfetta socorrensis is the dominant herbaceous
J.E. Martı´nez-Gómez, J.K. Jacobsen / Biological Conservation 116 (2004) 35–47
species (Martı́nez-Gómez et al., 2001). The dense and
intricate herbaceous layer may provide protection from
predators. We detected shearwaters landing in 22 of the
31 sampling stations above 500 m; most sightings were
concentrated in forested areas north and northwest of
Mount Evermann (Figs. 1 and 3). Below 500 m, we
observed few individuals flying above the stations; at
lower elevations, landings happened only at the naval
base, perhaps as a result of light attraction. Based on
these sightings, we obtained a rough estimate of a
minimum breeding population of ca. 1100 birds.
8.2. Predation
On Socorro, cats and red-tailed hawks preyed on the
endemic shearwater during the breeding season. During
41
our study we trapped 92 cats of which 40 (43%) were
found above 500 m. Overall, the majority of cat sign
was found south of the mountain summit where habitat
is highly degraded by sheep (Fig. 3). However, cats are
present in pristine areas to the north as indicated by cat
tracks detected at Playa Blanca. In 37 scats and 46 stomachs, the percentage of bird remains was significantly
higher in scats (2=11.33, df=1, P < 0.001) and stomachs ( 2=13.56, df=1, P < 0.001) collected above 500
m than in those below (Table 2). The high incidence of
bird remains indicates that cats pose a significant threat
to Townsend’s shearwater and Socorro’s avifauna
(Table 3). On the basis of shearwater remains in scat
samples, one ‘‘average’’ cat (sensu Apps, 1983) could
potentially kill ca. 36 female shearwaters if only scats
collected above 500 m were tallied (Table 4). Using
Fig. 3. Approximate location and number of shearwaters detected during this study. Five different breeding areas were found around Mount
Evermann above 800 m. The largest breeding grounds were found North and Northwest of the island’s summit where the vegetation has not been
damaged severely by introduced sheep. Black circles indicate the location of cat sign (scats, tracks, prey remains, captures) observed along the main
road, trails, and walking paths on the island.
J.E. Martı´nez-Gómez, J.K. Jacobsen / Biological Conservation 116 (2004) 35–47
42
only scats above 500 m for predation estimates on this
seabird is justified because of the elevation bias
abovementioned.
Table 2
Incidence of bird remains in cat scats and stomach contents below and
above 500 m of elevationa
Scats (m)
Bird remains
Present
Absent
Stomachs (m)
0–500
N=12
501–1000
N=25
0–500
N=35
501–1000 m
N=11
4
8
23 (8)
2
1
34
6 (4)
5
a
Numbers in parentheses indicate instances in which Townsend’s
shearwater remains were found.
Table 3
Percentage of different prey items found in cat scats and stomachs
collected at all elevations of the island during 1993–1996a
Scats
N= 100% Stomachs
37
N= 100%
46
Birds
Puffinus auricularis
Thryomanes sissonii
Parula pitiayumi
Mimodes graysoni
Pipilo maculatus
Mimus polyglottos
Reptiles and mammals
Urosaurus auriculatus
Mus musculus
Invertebrates
Schistocerca spp.
Scolopendra sp.
Beetles
27
8
7
3
2
2
1
7
6
1
31
26
10
1
7
4
2
1
15
14
1
20
19
6
2
73%
22%
19%
8%
5%
5%
3%
19%
16%
3
84%
70%
27%
3%
Birds
Puffinus auricularis
Pipilo maculatus
Parula pitiayumi
Reptiles and mammals
Urosaurus auriculatus
Mus musculus
Invertebrates
Schistocerca spp.
Scolopendra sp.
Gecarcinus planatus
15%
9%
4%
2%
33%
30%
2%
43%
41%
13%
4%
a
Notice the high incidence of bird remains in scats. Townsend’s
shearwater was the most common prey item found in scats and stomachs. Because some scats and stomachs contained several prey types,
their addition does not add up necessarily to the total or partial counts
for each category. Data from 1993 to 1994 (Martı́nez-Gómez and
Curry, 1996) were supplemented with findings from 1995 to 1996. No
scats were collected in 1997 because intense rain due to El Niño conditions washed away cat sign.
During the summer of 1993, many clusters of shearwater feathers were found on the forest floor in a manner suggestive of red-tailed hawk predation (c.f. Veitch
1985). Cats probably killed some of these birds first and
hawks scavenged their carcasses later. Shearwaters seem
to be a common item offered by red-tailed hawks to
their nestlings; remains of this seabird were found in
two inactive hawk nests and later in an active nest with
a nestling on 25 April 1994.
8.3. Population projections
Projections of the six scenarios modeled in this paper
and their demographic benchmarks are summarized in
Table 5 and Fig. 4. Besides the stable population, only
the projection under low predation (1 ‘‘average’’ cat)
had a population that persisted for more than 150 years.
Time to extincion was reached first (t=63) in the model
that incorporated high predation and habitat degradation. In the other models, population extinction took
more than 100 years. Under habitat degradation and
high predation, it took only 30 years for the number of
breeding females to drop below 100; a similar situation
was reached before 100 years in the models for habitat
degradation, high predation, and habitat degradation
with low predation (Table 5).
Thus, severe habitat loss combined with intensive
predation could have catastrophic consequences for
Townsend’s Shearwater in less than 100 years. Although
habitat degradation, high predation, and habitat degradation with low predation would allow population persistence for more than 100 years, this may not occur
because of the small number of breeding females present
at that time. Only very small predation rates would
allow population persistence and a large number of
breeding females for more than 150 years in spite of
declining conditions.
Annual rates of decrease when low and high predation levels were combined with habitat degradation were
only slightly higher than the addition of the individually
modeled factors; thus, it cannot be concluded that either
Table 4
Estimated number of female Townsend’s shearwaters killed by cats during a breeding season following an approach similar to that of Apps (1983)a
Year
1994
1995
1996
Mean
SD
All years
a
Scats found
>500 m
13
7
5
–
–
25
Proportion of scats
with shearwater
remains (p)
0.307
0.286
0.400
0.331
0.061
0.32
Shearwaters killed per
cat per breeding season
s=(p)(d)(r1)(k)(b)
66.312
61.776
86.400
71.496
13.105
–
Female shearwaters
killed per cat per
breeding season (s/2)
33.156
30.888
43.200
35.748
6.552
–
Total number of females killed T=(s/2) (N)
Low Predation
N=1 average cat
High Predation
N=10 average cats
33.156
30.888
43.200
35.748
6.552
–
331.560
308.880
432.000
357.480
65.524
–
Only cat scats collected above 500 m were used in these calculations because of a bias in prey contents due to elevation.
J.E. Martı´nez-Gómez, J.K. Jacobsen / Biological Conservation 116 (2004) 35–47
43
Table 5
Demographic benchmarks for the six models discussed in the text
Model
l
Annual rate of
decrease (%)
N t150
95% CI range
Time to
extinction
95% CI
range
Time to 100
last females
95% CI
range
Stable
Habitat Degradation (HD)
Low Predation (LP)
High Predation (HP)
HD & LP
HD & HP
1.00137
0.94322
0.99432
0.93625
0.93592
0.87311
–
5.68
0.56
6.37
6.40
12.68
10257
1
3863
1
0
0
7614–13521
0–8
2831–5144
0–8
0–2
0–0
–
147
–
142
130
63
–
118–177
–
106–172
107–152
53–75
–
71
–
58
62
30
–
66–67
–
53–63
58–67
28–31
predation or habitat degradation had a predominant
role in population decline. In all cases, sensitivity and
elasticity analyses obtained from the deterministic
models indicate that fertility and survival of the 6th age
class are the most critical elements in the demography of
this species (Table 6).
Another pattern derived from our projections is that
by modeling the number of survivors as a random
binomial number, confidence intervals are rather narrow because under a binomial distribution small populations will show less variance. Also, under low
predation conditions average population trajectories
show slightly larger numbers than these derived from a
deterministic run; in the remaining models deterministic
and average trajectories overlap.
9. Discussion
All the evidence gathered indicates that Townsend’s
shearwater is critically endangered. A decline in its
population can be inferred from its shrinking colony
and high predation rates. Our results confirm that previously reported colonies on Socorro below 800 m are
no longer occupied (e.g. Jehl and Parkes, 1982; Castellanos and Rodrı́guez-Estrella, 1992; Wehtje et al.,
1993; Llinas-Gutiérrez, 1994), and that cat predation
could affect seriously the demography of this species.
Available estimates of population size, including ours,
are less than ideal because none followed a demographic
methodology based on meticulous monitoring of breeding colonies. Jehl’s (1982) estimate of 1000 breeding pairs
was, after all, an educated guess. He used the number of
birds seen at one location to infer the number of individuals across the island. Implicitly, he assumed a homogeneous distribution of shearwaters at a certain
elevation. Population estimates by Spear et al. (1995),
although based on a regression model that accounts for
spatial heterogeneity, could be inaccurate because data
for their regression were gathered over several years.
Their approach probably introduced a temporal bias to
their analyses if the shearwaters were more abundant
during the initial years but declined subsequently. Interestingly, their estimate for P.a. newelli was within the
confidence limits of colony-based estimates obtained
independently (cf. Ainley et al., 2001).
The estimate of 1100 individuals presented in this
paper is certainly an underestimate because birds were
counted cautiously to avoid tallying individuals more
than once. Nevertheless, the dramatic change in the
amount of occupied habitat in recent decades (Jehl and
Parkes, 1982; Castellanos and Rodrı́guez-Estrella, 1992;
Wehtje et al., 1993; Llinas-Gutiérrez, 1994), and the
difference in order of magnitude between the estimates
of Spear et al. (1995) and ours very likely indicate a real
population decline. The trend is consistent, too, with the
results of our models.
Previous researchers probably failed to recognize the
high incidence of cat predation on the island’s avifauna
because of short surveys and sampling schemes concentrated below 500 m (Veitch, 1989, Rodrı́guezEstrella et al., 1991). Additionally, cat sign may be difficult to detect when relative humidity is high (June to
January approximately) because land crabs (Gecarcinus
planatus) effectively erase all tracks and destroy cat scats
overnight. Nonetheless, cat predation appears to be
pervasive on Townsend’s shearwater (Table 3), and the
number of shearwaters potentially killed by cats during
a breeding season is alarming (Table 4). Furthermore,
simple estimates for a species that produces one young
per year and reaches maturity at 5–6 years must maintain adult survival rates of at least 85%, and all mature
birds should breed successfully to uphold a viable
population (Perrins, 1991). Thus, even limited predation
could bring adult survival rates below that threshold
(e.g. Tomkins, 1985; Berruti, 1986; Cruz and Cruz,
1987; Seabrook, 1990; Ainley et al., 2001; Keith et al.,
2002).
The archipelago does not have large human settlements. Therefore, required conservation actions are
simply (1) the removal of introduced mammals and (2)
habitat restoration. The impact of severe predation and
habitat degradation will cease immediately once introduced mammals are removed. Losses due to the native
hawks should have a minor effect because of their
small population size (Walter, 1990). Restoration of
degraded habitats can be accomplished because preserved regions on Socorro have the necessary seed
44
J.E. Martı´nez-Gómez, J.K. Jacobsen / Biological Conservation 116 (2004) 35–47
banks from which plants can recolonize. On Clarion,
however, the impact of rabbits is pervasive and the
seed stock for many plants might be greatly reduced.
Enclosures of several sizes could be placed in degraded
regions; native plants can be seeded or transplanted to
these areas to constitute nuclei from which native
vegetation will spread. On Socorro, Dodonaea viscosa,
and Triumfetta socorroensis are good candidates for
Fig. 4. Demographic projections for the total population of female shearwaters incorporating demographic stochasticity, the impact of habitat
degradation, and predation. Confidence intervals (95%) were obtained through Monte Carlo simulations (10,000 runs). Under low predation the
deterministic run was slightly lower than the average trajectory obtained from simulations; in the remaining models these two trajectories are
practically the same. Numbers in parentheses in the middle projections represent survival rates of the last three age classes.
J.E. Martı´nez-Gómez, J.K. Jacobsen / Biological Conservation 116 (2004) 35–47
45
Table 6
Sensitivities (sij) and elasticities (eij) for the non-zero matrix elements in the six models discussed in the texta
Non-zero
elements
F15
F16
P21
P32
P43
P54
P65
P66
Stable Population
Habitat
Degradation
(HD)
Low Predation
(LP)
High Predation
(HP)
HD & LP
HD & HP
sij
eij
sij
eij
sij
eij
sij
eij
sij
eij
sij
eij
0.2805
0.2634
0.1051
0.0881
0.0772
0.0759
0.0699
0.6568
0.0054
0.0632
0.0686
0.0686
0.0686
0.0686
0.0632
0.5936
0.0180
0.4258
0.0500
0.0419
0.0367
0.0361
0.0349
0.8268
0.0011
0.0335
0.0346
0.0346
0.0346
0.0346
0.0335
0.7933
0.0289
0.2680
0.1053
0.0883
0.0774
0.0766
0.0705
0.6536
0.0055
0.0637
0.0693
0.0693
0.0693
0.0693
0.0637
0.5898
0.0386
0.3015
0.1112
0.0932
0.0817
0.0865
0.0783
0.6116
0.0074
0.0703
0.0777
0.0777
0.0777
0.0777
0.0703
0.5412
0.0187
0.4353
0.0503
0.0422
0.0369
0.0366
0.0354
0.8243
0.0012
0.0340
0.0351
0.0351
0.0351
0.0351
0.0340
0.7903
0.0276
0.5215
0.0561
0.0470
0.0412
0.0436
0.0418
0.7899
0.0017
0.0403
0.0420
0.0420
0.0420
0.0420
0.0403
0.7496
a
Numerical values in the table were rounded for presentation. Notice that in all cases the highest values are associated with the survival of birds 6
years old or older. In a declining population, the second largest sensitivity is the fertility value associated with the 6th age class; only in the stable
population is the second largest fertility value that of the 5th age class.
such a purpose. Introduced plants should be removed
at the same time.
Hopefully Townsend’s shearwaters will prospect for
burrows on Clarion once introduced mammals have been
eradicated (e.g. P. tenuirostris; Bradley et al., 1999).
Nonetheless, strategies to reintroduce the shearwaters
once mammals have been removed should be considered.
Some of the strategies proposed for the recovery of Newell’s shearwater could be implemented on Clarion (see
Telfer, 1983). Playbacks, olfactory baits, and decoys
should be attempted first. If these efforts fail, a translocation program must follow. Chicks that have not left their
burrows, and thus have not yet imprinted on their natal
island’s skies, are required (Telfer, 1983; Brooke, 1990).
Although our matrix projections are not based on
demographic parameters derived from Townsend’s
Shearwater and simplify complex demographic components of real life cycles, they show key demographic
elements that should be considered in conservation
actions. For instance, they demonstrate clearly the
importance of adult survival and reproduction and thus
the necessity to protect and preserve current breeding
areas. They also show that habitat degradation and cat
predation must be confronted at the same time. From a
conservation standpoint, attention to one threatening
factor would only be advisable if the impact of the other
is negligible; a situation that very likely does not occur on
Socorro.
Townsend’s shearwater demography will experience a
minimum change only if few cats prey on them. Based
on our trapping experience, we believe that no more
than a dozen cats may roam breeding grounds on
Socorro. In montane areas, the dense and intricate
understorey where the burrows are located provides
refuge from predators; most shearwaters are taken by
cats when they land in parts of the forest where the
understorey is practically absent. Under these conditions, a low but steady decline should be expected.
The pattern observed at Socorro differs from predation scenarios where target species lack protection from
vegetation and nesting areas are readily accessible to
predators (e.g. Black-vented shearwater; Keith et al.,
2002). In the latter conditions, even few predators may
cause significant damage to the population. The situation may be complicated for Townsend’s shearwater
because as sheep continue destroying vegetative cover
the impact of predation will increase dramatically.
Control efforts during the breeding season should be
implemented to minimize cat predation on shearwaters
and secure remaining breeding areas on Socorro from
further destruction by sheep. Special care should be
taken to avoid the risk of demographic instability.
Ultimately, the risk and timing of extinction will
depend on actual predation rates on adults and fledglings, the rate at which nesting habitat is lost, and on
how quickly the pool of mature birds found at sea
diminishes as times goes by. Intensive demographic
monitoring of Townsend’s shearwater will yield accurate estimates of survival rates, fecundity, productivity,
breeding phenology and movements that will allow
more realistic population projections. More importantly, such a program will aid in evaluating the performance of the different demotypes (sensu Ricklefs,
1991) in the population and the efficiency of eradication,
restoration, or translocation programs.
Acknowledgements
We would like to express our gratitude to the Mexican Navy for their continuous and generous support
throughout all years of this study. Financial, logistical
support, and/or equipment, were provided by the
American Museum of Natural History, the Cooper
Ornithological Society, the Association of Field Ornithologists, the American Ornithologist’s Union,
46
J.E. Martı´nez-Gómez, J.K. Jacobsen / Biological Conservation 116 (2004) 35–47
Sigma—Xi the Scientific Research Society, the Island
Endemics Institute, the California Academy of Sciences,
Villanova University, Humboldt State University, and
Idea Wild—Biodiversity Research Assistance Organization, the R.V. Odyssey of the Whale Conservation
Institute, Cetacean Society International, and the
National Geographic Society. A. Jesse and J. Dean
kindly offered measurements from nestlings in the California Academy of Sciences and the U.S. National
Museum. This manuscript benefited from the comments
of D. G. Ainley, R. Ricklefs, E. Hansen, A. Scheuerlein,
J. Sánchez, B. Tershy, B. Keitt, S. Fallon, J. Uribe, J.
Bollmer and two anonymous reviewers.
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