Winter bird gets the worm: consumption of earthworms (Lumbricidae) by striated caracaras (Phalcoboenus australis) in invasive Yorkshire fog (Holcus lanatus) in the Falkland Islands (Malvinas)

Abstract

Biological invasions can drive ecosystem change and alter predator ecology by providing trophic subsidies that mitigate the effects of seasonally pulsed resources. Striated Caracaras (Phalcoboenus australis) are near threatened, non-migratory falconids who inhabit the southern coasts of South America and the Falkland Islands (Malvinas) and feed on seasonally migratory colonial seabirds. Here we report the first multi-day observation of caracaras foraging extensively for earthworms (Lumbricidae) and beetle larvae (Coleoptera) in introduced Yorkshire fog (Holcus lanatus) on New Island, Falkland Islands. Our results suggest that invertebrates may be a more important winter resource than previously thought, and that caracaras benefit indirectly from introduced grasses in the Falklands, a relationship that merits special consideration when identifying ecological restoration plans.

Full text

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Polar Biology
https://doi.org/10.1007/s00300-021-02845-0
SHORT NOTE
Winter bird gets theworm: consumption ofearthworms (Lumbricidae)
bystriated caracaras (Phalcoboenus australis) ininvasive Yorkshire fog
(Holcus lanatus) intheFalkland Islands (Malvinas)
KatieJ.Harrington1 · JonathanMeiburg2· JenniferL.Houtz3
Received: 27 May 2020 / Revised: 3 March 2021 / Accepted: 9 March 2021
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021
Abstract
Biological invasions can drive ecosystem change and alter predator ecology by providing trophic subsidies that mitigate
the effects of seasonally pulsed resources. Striated Caracaras (Phalcoboenus australis) are near threatened, non-migratory
falconids who inhabit the southern coasts of South America and the Falkland Islands (Malvinas) and feed on seasonally
migratory colonial seabirds. Here we report the first multi-day observation of caracaras foraging extensively for earthworms
(Lumbricidae) and beetle larvae (Coleoptera) in introduced Yorkshire fog (Holcus lanatus) on New Island, Falkland Islands.
Our results suggest that invertebrates may be a more important winter resource than previously thought, and that caracaras
benefit indirectly from introduced grasses in the Falklands, a relationship that merits special consideration when identifying
ecological restoration plans.
Keywords Falconid· Ground-foraging· Invasive species Lumbricidae· Pulsed resources· Species conservation
Introduction
Biological invasions can drive ecosystem change and alter
predator ecology (Cameron and Bayne 2012). Some intro-
duced species can negatively impact native taxa through
direct predation or competition (Savidge 1987; Roemer etal.
2002), while others can positively impact predator popu-
lation growth by providing trophic subsidies (Barber etal.
2008; Pearson etal. 2009). In some island systems, preda-
tors have adapted to depend directly or indirectly on non-
native species (Roemer etal 2002; Bergstrom etal. 2009), a
relationship that merits special consideration when identi-
fying invasive eradication plans (Speziale and Lambertucci
2013), particularly as predators can structure ecological
communities (Legagneux etal. 2012) and may already be
facing conservation threats. Here we report an unintentional
effect of human-altered grassland ecology that may benefit
an endemic predator during the seasonal absence of migra-
tory prey.
Striated Caracaras (Phalcoboenus australis; hereafter
“caracaras”) are near threatened falconids who inhabit the
extreme southern coasts of South America and the Falkland
Islands (Malvinas; Balza etal. 2017; Reeves etal. 2018;
BirdLife International 2020). During summer, caracaras feed
on a seasonal resource pulse (sensu Yang 2010) associated
with colonial seabird populations (Strange 1996; Balza etal.
2017; Harrington etal. 2018). In winter, when most seabirds
migrate offshore, caracaras’ diets include native Upland
Geese (Chloephaga picta), the feces and carrion of resident
southern fur seals (Arctocephalus australis), southern sea
lions (Mirounga leonina), and Gentoo Penguins (Pygosce-
lis papua), beetles (Coleoptera), and subsidies available at
farms (Strange 1996; Rexer-Huber and Bildstein 2013; Har-
rington etal. 2018).
While Strange (1996) noted that caracaras consume inver-
tebrate prey throughout the year, the relative importance of
this dietary component throughout their range has never
been assessed, and invertebrate prey are absent from most
discussions about the species’ winter diet (Catry etal. 2008;
* Katie J. Harrington
katiejharrington@gmail.com
1 Acopian Center forConservation Learning, Hawk Mountain
Sanctuary, 410 Summer Valley Road, Orwigsburg,
PA17961, USA
2 1735 West Fitzhugh Road, DrippingSprings, TX78620,
USA
3 Department ofEcology andEvolutionary Biology, Cornell
University, Ithaca, NY, USA

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Autilio etal. 2019), despite that invertebrates form a part of
the diet of all other caracara species (Thiollay 1991; Travaini
etal. 2001; Donadio etal. 2007; Morrison etal. 2008; Solaro
and Sarasola 2012). Here we report a multi-day observation
of caracaras foraging for earthworms (Lumbricidae) and
beetle larvae in introduced grasslands on a formerly farmed
island.
Methods
New Island (51.72 S, 61.30W) is a 2200-ha nature pre-
serve in the southeast Falkland Islands (Malvinas), near the
southern tip of South America (Fig.1). The island retains
stands of native tussock grass (Poa flabellata), but is domi-
nated by stretches of diddle-dee (Empetrum rubrum) and
introduced Yorkshire fog (Holcus lanatus) and sheep’s sor-
rel (Rumex acetosella) (for a detailed description of New
Island, see Quillfeldt etal. 2008). Livestock were gradually
removed from the island between 1972 and 2006, during
which timethe breeding population of caracaras rebounded
from zero pairs (Strange 1996) to 86 pairs (Reeves and Bild-
stein 2018). During the austral summer, New Island supports
globally significant colonies of Thin-billed Prions (Pachyp-
tila belcheri), Southern Rockhopper Penguins (Eudyptes
chrysocome), and Black-browed Albatrosses (Thalassarche
melanophris), as well as Imperial Shags (Phalacrocorax
atriceps) andMagellanic Penguins (Spheniscus magellani-
cus), who allvacate the island during winter. The island
supports resident populations of Gentoo Penguins, Upland
Geese, southern fur seals, and southern sea lions year-round
(Strange etal. 2007).
From 4 to 10 August 2019 (austral winter), we conducted
a walking transect survey of New Island during daylight
hours (0900h to 1800h), recording caracara abundance,
location, age, and foraging behavior. We randomly selected
53 caracaras raking in the soil and conducted 30s focal sam-
pling (Altmann 1974), in which we stood at a 3m distance
and used binoculars to count the number and, when possible,
type of invertebrates consumed. Like many island endem-
ics, caracaras are generally unwary of human approaches
(Strange 1996), which created the unique opportunity to con-
duct the behavioral sampling described. We then surveyed
ten 625 cm2 plots of Yorkshire fog to record abundance of
invertebrate prey within the top 5cm of grass roots and soil.
We only sampled one grass plot per territory and targeted
areas adjacent to where we had observed caracaras digging.
Except for sheep’s sorrel, we only observed caracaras dig-
ging under Yorkshire fog, thus we restricted our sampling
to plots of Yorkshire fog for consistency. Earthworms were
later identified to the family using field markings from pho-
tographs (Reynolds 2020). To provide comparison between
the caracaras’ winter body condition and their summer
body condition, we trapped adult caracaras (aged following
Fig. 1 Map of New Island,
Falkland Islands (Malvinas),
prepared using the get_goog-
lemap function in the R package
ggmap (South 2017). Insets
show the location of the Falk-
land Islands to the northeast of
Cape Horn and the position of
New Island within the archi-
pelago, both prepared using the
ne_countries function in the R
package rnaturalearth (Kahle
and Wickham 2013). The thick
black line shows the locations
of the walking transect survey

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Strange 1996; n = 12 females, 5 males) using a mutton-
baited snarecarpet and recorded their mass to the nearest
25g using a hand-held scale (Harrington etal. 2018). We
visually assessed individual’s crop size, which we catego-
rized as not distended, partially distended, or distended,
allowing us to restrict our mass analysis to birds that did not
have distended crops. We combined these mass data with
data collected following the same protocol in March 2019
(n = 4 females, 7 males) and June 2014 (n = 13 females, 7
males; KH unpubl. data). Molecular sexing was performed
as described in Griffiths etal. (1998). Caracaras are size
dimorphic, with females being larger than males (Strange
1996), thus we grouped individuals by sex a priori. Austral
winter comprised June and August data, and austral sum-
mer comprised March data. We tested the effect of season
on mass by using a Welch Two Sample t test for our nor-
mally distributed female dataset and a Kruskal–Wallis test
for our non-normal male dataset. Statistical analyses were
performed using R version 3.5.2.
Results anddiscussion
During the island-wide survey, 70% of observed caracaras
(n = 284) were foraging. Of the foraging birds, 81% were
raking with their talons in dense mats of invasive Yorkshire
fog and sheep’s sorrel and feeding on invertebrates, often in
adult pairs or small groups of up to 15 individuals of all age
classes (Fig.2). Of caracaras not foraging on invertebrates,
10% were scavenging (i.e., walking and pecking at objects
along the shore), 7% were feeding on carcasses of Upland
Geese, and 3% were feeding on pinniped feces. During focal
sampling of caracaras raking in the soil, we recorded a feed-
ing rate of 4 ± 2 invertebrates per 30s. Within Yorkshire
fog survey plots (n = 10), we recorded 24 ± 29 readily vis-
ible invertebrates, with a maximum of 102 in a single plot
(earthworms: 19 ± 25, range: 3–86; beetle larvae: 5 ± 6,
range: 0–16; Fig.2C). Winter masses were lower by 1.2%
for adult females and 4.8% for adult males when compared
with summer masses. However, we found no significant dif-
ference in seasonal mass for females (winter 1685 ± 86g
[n = 25], summer 1706 ± 75g [n = 4]; Welch Two Sample t
test, t4 = 0.52, p = 0.63), nor for males (winter 1445 ± 81g
[n = 12], summer 1518 ± 150g [n = 7]; Kruskal–Wallis test,
H1 = 0.80, p = 0.37).
In the Falkland Islands (Malvinas), the direct and indirect
effects of sheep farming, including intense direct persecution
(Woods and Woods 1997), have reduced caracaras’ historical
distribution (Darwin 1845) to the outer islands of the archi-
pelago (Cawkell and Hamilton 1961; Strange 1996; Woods
2017). While the species is now protected and appears to be
recovering (Reeves and Bildstein 2018), they are not recolo-
nizing across their entire historical range, and the ecologi-
cal mechanisms that facilitate their recolonization of islands
remain unknown. A study of caracaras roosting near a set-
tlement on a farmed island posited that winter food stress
may limit the species’ recovery (Rexer-Huber and Bildstein
2013). However, caracaras throughout the Falklands inhabit
a wide range of landscapes, including formerly farmed (i.e.,
all stock has been removed) and “vegetationally pristine”
islands (Reeves and Bildstein 2018), which have differing
resource availability through winter. Though mass measure-
ments are not always a reliable indicator of body condition
or stress (King and Murphy 1985; Brown 1996), our results
suggest that invertebrates may be a more important winter
resource for caracaras than previously thought, and that it is
possible that winter may not be a time of food stress for all
caracaras in the Falklands. However, more work is needed
to establish baselines for body condition within the species.
In this study, we observed caracaras foraging for inverte-
brates almost exclusively within patches of introduced York-
shire fog and sheep’s sorrel and not in the island’s native
vegetation (e.g., feldmark and stands of tussac grass). We
hypothesize that the grasses introduced as pasturage and
Fig. 2 Adult Striated Caracaras (Phalcoboenus australis) raking in Yorkshire fog (Holcus lanatus; a and b) and earthworms (Lumbricidae) dug
from a study plot of Yorkshire fog (c). The darker soil patches in a and b indicate areas of grass that have already been dug out by caracaras

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the removal of sheep may have facilitated caracaras’ rapid
recolonization of New Island by mitigating the seasonal food
limitation imposed by migratory seabird prey and restoring
soil composition. While the Falkland Islands have several
native earthworms, introduced species are also common
throughout the islands (Reynolds and Jones 2006). Similar
winter foraging behavior by caracaras in introduced sheep’s
sorrel was observed on another formerly farmed island,
Steeple Jason (51.04 S, 61.21W), where all stock has been
removed and a survey indicated a stable year-round popula-
tion, despite the seasonal absence of the island’s large colo-
nies of albatrosses, penguins, and burrowing petrels (Woods
etal. 2012).
These observations are in sharp contrast to observations
from Saunders Island, an active sheep farm (see Harrington
etal. 2018 for description) that supports non-breeding cara-
caras in winter (Harrington etal. 2018) though, following
the 1964 government ban on direct persecution (Falkland
Islands Government 1999), has not been recolonized to the
extent of New Island (i.e., as of February 2019, there were
4 known nests on Saunders [KH unpubl. data] in compari-
son to 86 on New Island [Reeves and Bildstein 2018]). In
another winter diet study, Rexer-Huber and Bildstein (2013)
found beetle remains in caracara pellets at a communal roost
adjacent to the farm settlement on Saunders but did not
report earthworms. This may be due to the methodological
limitations of pellet analyses (Marti etal. 2007), although
it may also reflect lower invertebrate abundance due to soil
compaction from continued sheep farming (Langmaack
etal. 1999; Schon etal. 2017). Furthermore, during pre-
vious field seasons on Saunders, we have observed raking
for dipteran larvae in accumulated kelp wrack, though we
have observed little raking for soil invertebrates across four
winters from 2016 to 2019 (KH unpubl. data). It is possible
that the regular availability of subsidies at the island’s farm
settlement (see Harrington etal. 2018) is a more attractive
winter food source than terrestrially raked invertebrates;
however, this does not explain the limited recolonization of
Saunders Island.
We suggest further research into caracara winter resource
use on islands that have never been farmed, to better under-
stand how caracaras seasonally cope in the absence of
migratory prey and human food subsidies. Additionally, as
caracaras in the Falklands are an island-restricted species
of conservation concern, we suggest that the relationship
between caracaras and introduced species merits special
consideration when developing eradication and ecological
restoration plans.
Acknowledgements Funding was provided by Falklands Conserva-
tion, the Falkland Islands Government (FIG) Environmental Studies
Budget, the John Cheek Trust, and Hawk Mountain Sanctuary. We
thank the FIG Environmental Planning Department for permits and
the New Island wardens Alec and Giselle Hazell for logistical support.
We thank Keith Bildstein for beginning the long-term monitoring of
this species and Micky Reeves for collecting field data in 2014. We
also thank Paulo Catry, James Dwyer, and our reviewers, Ulises Balza
and an anonymous individual, for critical comments that improved
this manuscript. All research was conducted in accordance with the
FIG Conservation of Wildlife and Nature Ordinance under Research
License No: R22/2015. This is Hawk Mountain Contribution to Con-
servation Science No. 345.
Author contributions KJH conceptualized the study, administered
the project, and obtained project funding. KJH and JM conducted
fieldwork. JLH analyzed genetic data. KJH analyzed behavioral data.
KJH wrote and prepared the original manuscript. KJH, JM, and JLH
reviewed and edited the manuscript. All authors approved the submit-
ted manuscript.
Data availability Data are available upon request.
Declarations
Conflict of interest The authors declare no competing or financial in-
terests.
Ethical approval All capture, handling, and instrumentation proce-
dures were approved by the San Jose State University Institutional
Animal Care and Use Committee protocol (#1054) and conducted
under the Conservation of Wildlife and Nature Ordinance of 1999,
Sect.9, License to carry out Scientific Research permit (#R22/2015,
Falkland Islands Government). Informed consent was not applicable.
We caught a total of 28 caracaras for this study and complemented our
dataset with existing data from an additional 20 birds. We observed
no adverse effects of trapping and handling. During our subsequent
breeding success surveys, we observed no long-term effects of the birds
having been previously trapped.
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