Effects of Horseshoe Crab Harvest in Delaware Bay on Red Knots: Are Harvest Restrictions Working?
ABSTRACT Each May, red knots (Calidris canutus rufa) congregate in Delaware Bay during their northward migration to feed on horseshoe crab eggs (Limulus polyphemus) and refuel for breeding in the Arctic. During the 1990s, the Delaware Bay harvest of horseshoe crabs for bait increased 10-fold, leading to a more than 90% decline in the availability of their eggs for knots. The proportion of knots achieving weights of more than 180 grams by 26–28 May, their main departure period, dropped from 0.6–0.8 to 0.14–0.4 over 1997–2007. During the same period, the red knot population stopping in Delaware Bay declined by more than 75%, in part because the annual survival rate of adult knots wintering in Tierra del Fuego declined. Despite restrictions, the 2007 horseshoe crab harvest was still greater than the 1990 harvest, and no recovery of knots was detectable. We propose an adaptive management strategy with recovery goals and annual monitoring that, if adopted, will both allow red knot and horseshoe crab populations to recover and permit a sustainable harvest of horseshoe crabs.
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ABSTRACT: Since 1985, avian influenza virus surveillance has been conducted annually from mid-May to early June in charadriiform species from the families Scolopacidae and Laridae (shorebirds and gulls) at Delaware Bay in the northeast United States. The mass migrations of shorebirds, gulls and horseshoe crabs (Limulus polyphemus) coincide at that time, and large numbers of migrating birds pause at Delaware Bay to feed on horseshoe crab eggs deposited at the high-tide line. Influenza viruses are consistently isolated from charadriiform birds at Delaware Bay, at an overall rate approximately 17 times the combined rate of isolation at all other surveillance sites worldwide (490 isolates/9474 samples, 5.2% versus 49 isolates per 15,848 samples, 0.3%, respectively; Proportion test, p < 0.0001). The likelihood of isolating influenza viruses at Delaware Bay is dependent on the presence of ruddy turnstone (Arenaria interpres) at the sampling site (G-test of independence, p < 0.001). The convergence of host factors and environmental factors results in a unique ecological 'hot spot' for influenza viruses in Charadriiformes.Proceedings of the Royal Society B: Biological Sciences 11/2010; 277(1699):3373-9. · 5.68 Impact Factor
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ABSTRACT: There are nine serotypes of avian paramyxovirus (APMV), including APMV-1, or Newcastle disease virus. Although free-flying ducks and geese have been extensively monitored for APMV, limited information is available for species in the order Charadriiformes. From 2000 to 2005 we tested cloacal swabs from 9,128 shorebirds and gulls (33 species, five families) captured in 10 states within the USA and in three countries in the Caribbean and South America. Avian paramyxoviruses were isolated from 60 (0.7%) samples by inoculation of embryonating chicken eggs; isolates only included APMV-1 and APMV-2. Two isolates (APMV-2) were made from gulls and 58 isolates (APMV-1 [41 isolates] and APMV-2 [17 isolates]) were made from shorebirds. All of the positive shorebirds were sampled at Delaware Bay (Delaware and New Jersey) and 45 (78%) of these isolates came from Ruddy Turnstones (Arenaria interpres). The APMV-1 infection rate was higher among Ruddy Turnstones compared with other shorebird species and varied by year. Avian paramyxovirus-2 was isolated from two of 394 (0.5%) Ruddy Turnstones at Delaware Bay in 2001 and from 13 of 735 (1.8%) Ruddy Turnstones during 2002. For both APMV-1 and APMV-2, infection rates were higher among Ruddy Turnstones sampled on the south shore of Delaware Bay compared to north shore populations. This spatial variation may be related to local movements of Ruddy Turnstones within this ecosystem. The higher prevalence of APMV in Ruddy Turnstones mirrors results observed for avian influenza viruses in shorebirds and may suggest similar modes of transmission.Journal of wildlife diseases 04/2010; 46(2):481-7. · 1.27 Impact Factor
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ABSTRACT: A population decline of the western Atlantic red knot (Calidris canutus rufa) has been linked to food limitation during the spring migratory stopover in Delaware Bay, USA. The stopover ecology at potential alternative sites has received little attention. We studied factors affecting red knot habitat selection and flock size at a coastal stopover site in Virginia in 2006–2007. The most common potential prey items were coquina clams (Donax variabilis) and crustaceans. Red knot foraging sites had more clams and crustaceans than unused sites in 2006. Prey abundance increased during the 2007 stopover period and remained high after the red knot peak. Red knot flock size in 2007 increased with mean clam shell length, and probability of flock presence decreased with increasing distance from night use locations. Our results suggest that red knots preferred coquina clams and that these clams were not depleted during the stopover period in 2007. Thus prey abundance did not appear to be a population-limiting factor at this coastal stopover site in Virginia in that year. Protection of coastal sites outside of Delaware Bay, many of which have been altered by human development, would likely benefit red knot population recovery, as they can apparently provide abundant food resources during at least some years. Keywords Calidris canutus -Barrier islands-Habitat selection-Red knots-Shorebirds-Virginia10/2009; 151(2):355-364.
mus). For red knots,it is the final stop before a single direct
1992, Harrington 2001), where, on arrival in early June,
the flight to the Arctic and survival and successful breeding
(Baker et al.2004,Morrison and Hobson 2004,Morrison et
gratory stopover for six shorebird species—red knot,ruddy
turnstone (Arenaria interpres), sanderling (Calidris alba),
semipalmated sandpiper (Calidris pusilla), dunlin (Calidris
with peak counts of more than 400,000 individuals; esti-
mates are that more than 1 million shorebirds used the bay
ew World red knots (Calidris canutus rufa) migrate an-
Western Hemisphere Shorebird Reserve Network (Myers et
spectacular shorebird stopovers, comparable with the Cop-
Yellow Sea in Asia. Delaware Bay had also spawned an eco-
tourism industry with an estimated worth of $34 million
(Eubanks et al.2000).
dance and ease of collection when spawning made them a
prime target as bait for an emerging conch fishery in the
early 1990s.In the five years between 1992 and 1997,the re-
ported harvest of crabs grew 20-fold from about 100,000 to
more than 2 million (figure 2),at an estimated value of $11
the number of hand-collecting permits for Delaware grew
from 10 in 1991 to 132 in 1997, indicating a large increase
Effects of Horseshoe Crab Harvest
in Delaware Bay on Red Knots: Are
Harvest Restrictions Working?
LAWRENCE J. NILES, JONATHAN BART, HUMPHREY P . SITTERS, AMANDA D. DEY, KATHLEEN E. CLARK, PHILLIP W.
ATKINSON, ALLAN J. BAKER, KAREN A. BENNETT, KEVIN S. KALASZ, NIGEL A. CLARK, JACQUIE CLARK, SIMON
GILLINGS, ALBERT S. GATES, PATRICIA M. GONZÁLEZ, DANIEL E. HERNANDEZ, CLIVE D. T. MINTON, R. I. GUY
MORRISON, RONALD R. PORTER, R. KEN ROSS, AND C. RICHARD VEITCH
polyphemus) and refuel for breeding in theArctic.During the 1990s,the Delaware Bay harvest of horseshoe crabs for bait increased 10-fold,leading
to a more than 90% decline in the availability of their eggs for knots. The proportion of knots achieving weights of more than 180 grams by 26–28
May, their main departure period, dropped from 0.6–0.8 to 0.14–0.4 over 1997–2007. During the same period, the red knot population stopping in
Delaware Bay declined by more than 75%, in part because the annual survival rate of adult knots wintering in Tierra del Fuego declined. Despite
restrictions,the 2007 horseshoe crab harvest was still greater than the 1990 harvest,and no recovery of knots was detectable.We propose an adaptive
management strategy with recovery goals and annual monitoring that, if adopted, will both allow red knot and horseshoe crab populations to
recover and permit a sustainable harvest of horseshoe crabs.
Keywords: red knot, Calidris canutus rufa, Delaware Bay, horseshoe crab, Limulus polyphemus
www.biosciencemag.orgFebruary 2009 / Vol. 59 No. 2 • BioScience 153
BioScience 59: 153–164. ISSN 0006-3568, electronic ISSN 1525-3244. Request permission to photocopy or reproduce article content at the University of
California Press’s Rights and Permissions Web site at www.ucpressjournals.com/ reprintinfo.asp. doi:10.1525/bio.2009.59.2.8
dramatic decrease in spawning crabs and thus in the avail-
bird numbers on Delaware Bay were soon falling fast; peak
for 1998–2002 (figure 3,box 1).
(ASMFC) began to implement restrictions,and some states
implement restrictions (ASMFC 1998, 2006a). The notable
Early restrictions, such as stopping the harvest during the
ing the disturbance to feeding birds, but
they did little to reduce the harvest. By
crabs to about 600,000, from a high of
more than 2 million. Although the 2004
harvest was only a quarter of the 1998
peak, it was still well above harvests
increase in the early 1990s (figure 2). In
2006, concern that harvest restrictions
review by the ASMFC stock assessment
vest still exceeded production (ASMFC
2006b).Since May 2008 there has been a
moratorium on the harvest of female
torium on the harvest of all horseshoe
crabs in New Jersey.
Abundant horseshoe crab eggs are a
particularly valuable food resource for
time-stressed, long-distant migrants, in-
cluding red knot, ruddy turnstone, and
they are easily digested and metabolized
into fat and protein (Castro and Myers
1993,Haramis et al.2007).The digestive
from South America are reduced in size
(Piersma and Gill 1998) and are initially
inadequate to support feeding on knots’
usual prey—hard-shelled bivalves (e.g.,
rich horseshoe crab eggs allows birds to
feed at high rates when they arrive, re-
build their organs and muscles, and
recorded in knots (Atkinson et al. 2007,
Haramis et al. 2007). Consequently, the
stopover duration of Delaware Bay knots is much shorter
(10 to 14 days) than comparable stopovers in other parts
of the world (21 to 28 days) (Piersma et al.2005).However,
is that no similar,easily digested alternative food is available
(particularly the Florida wintering population [Niles et al.
ing to alternative prey does not seem to be an option.Knots
migrating long distances from Tierra del Fuego would have
to arrive earlier and stay longer in Delaware Bay to refuel
adequately and depart on time,as there is only a short time
window for successful breeding in theArctic.
154 BioScience • February 2009 / Vol. 59 No. 2www.biosciencemag.org
Figure 1.Delaware Bay and the main parts of the shore used by red knots (dark lines)
during their spring migration.The inset portrays the entire migration route from
Tierra del Fuego in Chile and Argentina to the Arctic.
the beach surface (Botton et al. 1994), a depth that is in-
individual females unearth existing egg masses when laying
their own eggs, bringing eggs to the surface, where they are
available to shorebirds. Eggs are also brought to the surface
by wave action, which loosens sand and eggs (Botton et al.
Eggs brought to the surface are lost to horseshoe crab re-
quickly desiccate and die.As early as 1997,concern over the
have focused particularly on red knots, ruddy turnstones,
Bay belong to separate populations that breed in the central
Canadian Arctic and winter in Tierra del Fuego, northern
Bay and the populations in all three wintering areas have
suffered a major collapse (Morrison et al. 2004, Niles et al.
Rufa is listed as endangered under the Bonn Convention
and is proposed for endangered status in Brazil (Niles et al.
mined that rufa warranted “threatened” listing under the
Endangered Species Act (50 C.F.R.17),but chose not to list
it because of insufficient staff and fiscal resources,as well as
In April 2007, the Committee on the Status of Endangered
Wildlife in Canada classified the southern wintering popu-
and Florida populations as threatened (COSEWIC 2007).
In this article we review more than a decade of studies of
red knots, horseshoe crabs, and horseshoe crab eggs in
Delaware Bay. We ask whether, after nine years of reduced
horseshoe crab harvest, conditions for knots in Delaware
Bay have improved. We suggest a recovery paradigm—a
series of assumptions about how the recovery of horseshoe
crabs and knots can be accomplished—and propose recov-
ery parameters that should be monitored to ensure that re-
covery proceeds as anticipated. Finally, we describe current
www.biosciencemag.org February 2009 / Vol. 59 No. 2 • BioScience 155
Figure 2.Harvest of horseshoe crabs reported by mid-Atlantic
states.Gray bars represent the estimated harvest,according to
interviews with state marine fish biologists from Delaware and
New Jersey (reliable harvest reports are not available for years
prior to 1997).Black bars represent the sum of the harvest
reported to the Atlantic States Marine Fisheries Commission by
New Jersey,Delaware,Maryland,Virginia,and New York.
Figure 3.Mean peak counts of red knots observed on aerial
surveys of Delaware Bay 1986–2007 in five- to six-year
periods (bars are ±95% confidence intervals).
The conflict between fishermen using horseshoe crabs as bait
and conservationists demanding a healthy shorebird stopover
mirrors other conflicts around the United States over multiple
uses of resources: the spotted owl and forest products industry,
wolves and sport hunters inAlaska,and Pacific salmon and
water resources in the Pacific Northwest.A teachers’curricu-
lum program called“Green Eggs and Sand”takes advantage of
the controversy on the Delaware Bay to provide teachers with a
window into the complexities of resource conflicts and the
methods used to resolve them.Working with biologists,the
program creators designed a curriculum guide to help middle-
school and high-school teachers learn of the complex life his-
tory of each animal and their interrelationships.Then they
focus on how fishery management decisions are made,the
resource-use conflict,and the difficulties of resolution.They
conclude with a discussion of similarly contentious issues
throughout the country.For more on this program,contact
Cindy Etgen at www.dnr.state.md.us/education/ are/ges.html.
Box 1. “Green Eggs and Sand”: A Resource for Teachers.
Bay, and show that with minor modification, they can pro-
vides an excellent opportunity to employ an adaptive man-
agement approach (Williams et al. 2001) and stress those
needed to ensure the sustainability of the horseshoe crab
Horseshoe crabs: Trends in population
size and the density of their eggs
Several surveys during the past 20 years (ASMFC 2004) of
adult horseshoe crabs in Delaware Bay have led to various
Smith 2007, Sweka et al. 2007). To illustrate the population
trend, we use standardized data collected since 1990 by
Delaware Division of Fish and Wildlife.A 30-foot trawl net
was towed for 20 minutes (covering about 2 km), once per
month from March to December, on each of nine transects
criticized in anASMFC peer review in 1998 (ASMFC 1998)
in 2000; we report on that survey in this article.
The Delaware 30-foot trawl surveys showed a decline of
88% (r2= 0.76, p < 0.001) in the mean number of crabs
of the late 1990s,but those figures are still much lower than
the levels of the early 1990s. It takes 10 years for horseshoe
crabs to become sexually mature (Schuster and Sekiguchi
the increase in 2006 and 2007 a consequence of harvest re-
strictions that began in 1998.Therefore,a recovery of adult
horseshoe crabs may be under way.
in horseshoe crab numbers started in 2006.Hata (2008) re-
shoe crabs. The mean catch was 35.0 in 2005, 65.1 in 2006,
from 2005 to 2006–2007. Counts of spawning crabs have
been made since 1999 on Delaware Bay beaches (Michels et
per square meter (m2) increased from 3.23 (standard error
in 2007, but the mean number of females per m2showed
little change: 0.82 (SE 0.07) to 0.99 (0.07) to 0.89 (0.07),
sidering the long period of sexual maturation, results from
more years of surveying are needed to measure the strength
and persistence of this trend.
1992 in Delaware Bay, Botton and colleagues (1994) esti-
mated the density of eggs in the upper 5 cm of sediments
age densities per m2ranged from 3125 to 721,354 (mean
gan in 1996 used varying survey methods in its first four
3-meter (m) intervals between the high- and low-tide lines
assuming that in 1990 and 1991,it equaled the mean of the
3406, a decline of about 98% from the estimated density in
the early 1990s. This estimate of the scale of decline should
numbersof crabshavedeclined.Inviewof theevidencethat
of an increase in egg density. However, if horseshoe crab
populations are recovering, as suggested by trawl surveys,
egg densities should begin to improve within the next few
156 BioScience • February 2009 / Vol. 59 No. 2www.biosciencemag.org
Figure 4.Number of adult horseshoe crabs caught on standard-
ized surveys in Delaware Bay conducted by the Delaware
Division of Fish and Wildlife.An exponential curve is fitted to
the years 1990–2005.
Red knots: Trends in population size
wintered in southern South America from Tierra del Fuego
north to Río Colorado in Patagonia (Morrison and Ross
1989, Morrison et al. 2004, Baker et al. 2005a). Estimates of
wintering numbers there were made in 1985 using aerial
surveys (Morrison and Ross 1989), in 1995 using capture-
or their numbers over- or underestimated. Consistency of
method and timing keeps such errors to a minimum.
Tierra del Fuego population fell by almost 50% between
of 85% for 1994–1995 through 1997–1998 to 56% for
1998–1999 through 2000–2001, and recruitment into the
at 25,000 to 30,000 birds between 2002 and 2004,the popu-
lation again plunged to between 17,000 and 18,000 in
2005–2007 and then to 14,800 in 2008 (COSEWIC 2007,
Niles et al.2008).
Smaller numbers of knots winter in northern Brazil at
Maranhão and in the southeastern United States, mainly
Florida. Surveys of Maranhão revealed 8324 birds in 1985
and about 3000 in 2006 (Niles et al.2008).
ularly on the Florida gulf coast,have not been surveyed sys-
tematically. Niles and colleagues (2008) suggested that the
emphasized uncertainty about the true number. In Florida,
1979, between 4000 and 5000 in 2004, and 2142 in 2006
ple winter survey of southeastern United States (Niles et al.
ied from hundreds to nearly 5000,but there are insufficient
during winter from South Carolina and farther north and
Since 1986,fourtosixweekly aerialsurveys of shorebirds
gration in May and early June. The survey covers most bay
sey, where small numbers can be found foraging; therefore,
it does not record total numbers but provides an index of
stopover population size.Peak aerial counts (figure 3) show
peak (12,375) was the lowest ever recorded.
Red knots: Trends in weight gain
Since 1997, red knots have been captured, banded, and
later. Peak numbers usually occur during 14–28 May, after
their weights have shown considerable year-to-year varia-
trend (figure 7a). However, during 21–27 May, and 28 May
to 3 June, when most birds depart, weights have shown a
www.biosciencemag.org February 2009 / Vol. 59 No. 2 • BioScience 157
Figure 5.Estimated density of horseshoe crab eggs (eggs per
square meter in the top 5 centimeters of sand) on Delaware Bay
beaches.Data for 1990–1991 are from Botton and colleagues
(1994).The y-axis is log scale,and the bars are ±1 standard
error.Data on variation are not available for 1990–1991 or
1996–1999,so error bars cannot be shown.
Figure 6.Number of red knots counted during surveys of their
wintering grounds in southern South America,1985 and
2000–2008,and estimated using capture-recapture methods
in 1995 (González et al.2004).