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Earthworms in the diet of herring gulls (Larus argentatus) breeding on an off-shore island Pennycott, Tom W.; Grant, David; Nager, Ruedi G.
Published in: Bird Study
DOI: 10.1080/00063657.2020.1743232
Published: 06/08/2020
Document Version Peer reviewed version
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Citation for published version (APA): Pennycott, T. W., Grant, D., & Nager, R. G. (2020). Earthworms in the diet of herring gulls (Larus argentatus) breeding on an off-shore island. Bird Study, 67(1), 131-134. https://doi.org/10.1080/00063657.2020.1743232
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Download date: 02 Oct 2021 “This is an Accepted Manuscript of an article published by Taylor & Francis Group in Bird Study on 06/04/2020, available online: https://doi.org/10.1080/00063657.2020.1743232.” 1 Earthworms in the diet of Herring Gulls (Larus argentatus) breeding on an off-shore
2 island
3 Tom W. Pennycott, Browncarrick Drive, Ayr, KA7 4JA, Scotland.
4 David Grant, University of the West of Scotland, Ayr Campus, Ayr, KA8 0SX, Scotland.
5 Ruedi G. Nager, Graham Kerr Building, IBAHCM, University of Glasgow, G12 8QQ,
6 Scotland.
7 Short title: Earthworms and Herring Gulls
8 Key words (in addition to those in title): regurgitated pellets; terrestrial vegetation; chaetae,
9 rainfall
10 Email of correspondence author: [email protected]
11
12 Summary
13 Pellets of indigestible material regurgitated by Herring Gulls breeding on Lady Isle, Firth of
14 Clyde, Scotland, were collected in 2018 and 2019 and examined for earthworm chaetae.
15 Nearly two-thirds (65.6%) of the 314 pellets came from gulls that had consumed one or more
16 earthworms. Significantly fewer pellets (57.6%) contained chaetae in 2018, a relatively dry
17 May to July, than in 2019 (72.0%) when rainfall was close to the long-term average for May
18 to July. There were significant associations between the presence of large quantities of
19 terrestrial vegetation in the pellet and the detection of large numbers of earthworm chaetae
20 and/or fragments of terrestrial arthropods, suggesting that recent consumption of these food
21 items is likely when pellets contain large quantities of vegetation.
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22 Earthworms in the diet of Herring Gulls (Larus argentatus) breeding on an off-shore
23 island
24
25 The Herring Gull population in the UK is currently in decline and has been since the 1970s,
26 warranting its red-listed status (Eaton et al. 2015). The exact reasons for this population
27 decline are unknown but changes in food resources could be one possible explanation
28 (Mitchell et al. 2004). Any advances in the understanding of the diet of this species are
29 therefore to be regarded as positive.
30 Information about the diet of Herring Gulls in southwest Scotland and nearby Northern
31 Ireland, based on analysis of regurgitated pellets, has been provided by Melville (1974),
32 Nogales et al. (1995) and O’Hanlon et al. (2017). However, the methodology used in these
33 studies did not include examination for the remains of earthworms (Class Oligochaeta,
34 Family Lumbricidae). Earthworms were recognised as a source of food for gulls as long ago
35 as the 1920s and 1930s (Portielje 1928, O’Mahony 1935) and are potentially highly nutritious
36 (Edwards 1985). Most parts of an earthworm are easily digested after being eaten by a bird
37 or mammal, but the chaetae (bristle-like structures found in their hundreds on the outer
38 surface of earthworms) are not digested and are passed out in the faeces or regurgitated in
39 pellets where they can be detected using appropriate methodology (Coulson & Coulson
40 2008).
41 Within southwest Scotland, the Clyde Basin is an important area for breeding Herring Gulls,
42 and Lady Isle (55.53°N, 4.73°W), a very small (4.4 hectares) unpopulated island within the
43 Clyde Basin 5.6 km off the Ayrshire coast, hosts a large and, in the Scottish context,
44 significant Herring Gull colony, with approximately 4-5% of the total Scottish Herring Gull
45 breeding population (Grant et al. 2013). Lady Isle also has smaller numbers of breeding
46 Lesser Black-backed Gulls L. fuscus and Great Black-backed Gulls L. marinus (Grant et al.
47 2013).
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48 Determining whether Herring Gulls on Lady Isle consume earthworms is important in studies
49 looking at resource use by gulls in this area of Scotland, to establish baseline data for the
50 occurrence of this food item in their diet and to complement previous studies in this region by
51 Nogales et al. (1995) and O’Hanlon et al. (2017). In addition, many previous researchers
52 (Harris 1965; Vernon 1970; Melville 1974; Nogales et al. 1995; Coulson & Coulson 2008;
53 Lindborg et al. 2012; O’Hanlon et al. 2017) have reported the presence of large quantities of
54 terrestrial vegetation in pellets produced by different species of gulls. In most of these
55 studies no attempts were made to look for earthworm chaetae and the significance of the
56 vegetation was unclear. Coulson & Coulson (2008) did, however, propose that such
57 terrestrial vegetation was accidentally consumed when gulls were foraging for earthworms
58 and insects. Here, using an enhanced method of pellet analysis, we explored the importance
59 of earthworms in the diet of Herring Gulls breeding in a coastal colony, and tested a possible
60 association between the presence of large quantities of terrestrial vegetation and the
61 detection of large numbers of earthworm chaetae in Herring Gull pellets.
62 On Lady Isle, Herring Gulls nest predominantly on the periphery of the island whereas
63 Lesser and Great Black-backed Gulls occupy slightly higher ground with more vegetation in
64 the interior (Grant et al. 2013). During the 2018 and 2019 breeding seasons, we collected
65 pellets from rocks, nests or the vicinity of nests in areas on Lady Isle in which Herring Gulls
66 breed (139 in May – July 2018, 175 in May – July 2019) and stored them in a deep freeze
67 prior to testing. Each pellet was defrosted and left for at least two hours in a 100 ml container
68 filled with water. The pellets were teased apart within the water, agitated vigorously for two
69 minutes with glass beads, and the contents passed through a disposable coarse sieve
70 (mesh size 1-2 mm) into a collecting container. Larger items remained in the sieve and small
71 items such as earthworm chaetae passed through the sieve into the washings. A 45 ml
72 container with a conical base was filled with some of the washings and allowed to stand for
73 at least 20 minutes to permit sedimentation of any earthworm chaetae present. Using a
74 disposable transfer pipette, six drops (approximately 300 µl) of sediment were transferred to
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75 a glass slide, glass coverslips added, and the slides examined using a binocular microscope
76 with transmitted light at a magnification of x100 (x10 eyepiece and x10 objective lens). If the
77 sediment was very thick, three drops of sediment were mixed with three drops of water on
78 the slide. The number of earthworm chaetae detected in 300 µl of sediment was recorded as
79 0, 1-50 or over 50. This threshold was chosen pragmatically after a pilot study in 2017 used
80 this methodology to determine chaetae numbers in 36 gull pellets, in which small numbers
81 (1-50) possibly reflected an earthworm meal in the recent past and larger numbers (>50 in
82 300 µl of sediment) suggested more recent consumption of one or more earthworms.
83 The contents of the sieve were dried and examined grossly and with a binocular dissecting
84 microscope (magnification range 7-45) and the main component(s) identified, quantified and
85 recorded, including the presence of large quantities (comprising more than 40% of the pellet)
86 of coarse terrestrial vegetation such as leaves, stems and roots.
87 When viewed under transmitted light at x100 magnification, earthworm chaetae were clearly
88 visible as long, narrow, yellowish, glassy translucent structures with faint transverse
89 striations. Most had an elongate sigmoid shape, with up-turning and down-turning of
90 dissimilar opposite ends and with a slightly thickened band approximately one third along
91 their length (Figure 1). Statistical comparisons were calculated by Pearson’s chi-squared test
92 with Yates’ correction, using an on-line statistical calculator
93 (https://www.socscistatistics.com/tests/chisquare/).
94 We collected and analysed a total of 314 pellets. The commonest items making up at least
95 25% of the bulk of a pellet were anthropogenic debris such as waste food, plastic, paper,
96 aluminium foil and glass (32.2% of pellets), cereal husks and/or kernels (30.6%) and marine
97 items such as fragments of fish, crabs and langoustines (10.2%). Evidence of earthworm
98 consumption was found in 206 out of 314 (65.6%) pellets: 98 pellets (31.2%) contained large
99 numbers (>50 in 300 µl of sediment) of chaetae, and smaller numbers (1-50 chaetae in 300
100 µl of sediment) were found in a further 108 pellets (34.4%). Earlier studies on the diet of
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101 Herring Gulls in the Firth of Clyde did not use methods that would readily detect earthworm
102 chaetae in pellets (Nogales et al. 1995, O’Hanlon et al. 2017), but using different
103 methodology we found earthworm chaetae in two-thirds of pellets. This is probably an
104 overestimate of the frequency of earthworms in the diet as chaetae could be detected in the
105 faeces of Choughs Pyrrhocorax pyrrhocorax for at least twelve faecal evacuations after
106 consumption of an earthworm (Meyer et al. 1994), and the detection of small numbers of
107 chaetae probably reflected carry-over of chaetae from an earlier meal. Thus, the frequency
108 of pellets with larger numbers of chaetae (31.2%) better reflects the contribution of
109 earthworms to the diet of Herring Gulls, although our threshold of >50 chaetae in 300 µl of
110 sediment was chosen pragmatically and may require further study. Coulson & Coulson
111 (2008) found a high frequency of pellets containing earthworm chaetae (55.2%) in Lesser
112 Black-backed Gulls breeding in an inland urban colony in southwest Scotland, and Sibly &
113 McCleery (1983) found that earthworms were one of the four most important food sources
114 for a coastal colony of Herring Gulls close to an agricultural landscape in northwest England.
115 This variation in the presence of earthworms in diet samples may be due to differences in
116 accessibility to areas rich in earthworms and/or methodological differences between studies.
117 The findings from the current study on Lady Isle demonstrate that the prevalence of pellets
118 containing chaetae is much greater than previous research into the diet of Herring Gulls in
119 Scotland and Northern Ireland had suggested and supports the conclusion of Coulson &
120 Coulson (2008) that the methodology employed is key to determining the presence or
121 absence of earthworm chaetae in gull pellets.
122 Within-year comparison of pellets was not considered valid because some pellets containing
123 tightly wrapped terrestrial vegetation can remain relatively intact for over six weeks (T.
124 Pennycott, unpubl. data), and thus pellets collected in the chick-rearing phase could have
125 been produced during the egg incubation stage. Instead, between-year comparisons were
126 carried out. Significantly fewer pellets contained chaetae in 2018 (80 out of 139 pellets,
127 57.6%) than in 2019 (126 out of 175 pellets, 72.0%) (Pearson’s chi-squared test with Yates’
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128 correction, ꭕ2=6.54, n=314, P<0.05). Similarly, fewer pellets contained large numbers of
129 chaetae in 2018 (22 out of 139 pellets, 15.8%) than in 2019 (76 out of 175 pellets, 43.4%)
130 (Pearson’s chi-squared test with Yates’ correction, ꭕ2=26.22, n=314, P<0.01). These
131 differences possibly reflect the effects of weather conditions on earthworm numbers and
132 accessibility, with earthworms becoming more available after wet conditions (Vernon 1972,
133 Kruuk 1978). Total rainfall recorded at Prestwick (approximately 6.5 km from Lady Isle) for
134 May-July 2018 was 135 mm (the driest May-July recorded at Prestwick between 2010 and
135 2019), whereas total rainfall for May-July 2019 was 215 mm, close to the ten-year Prestwick
136 May-July mean of 212 mm (Scottish Environment Protection Agency
137 https://apps.sepa.org.uk/rainfall/data/index/344764 Accessed 26/08/19). Thus, the wetter
138 weather in 2019 could explain the higher proportion of pellets with earthworm chaetae in that
139 year.
140 In 89 pellets (28.3%), coarse terrestrial vegetation comprised at least 40% of the bulk of the
141 pellet (Figure 2). There was a highly significant association between the presence of much
142 coarse terrestrial vegetation and large numbers (>50 in 300 µl of sediment) of earthworm
143 chaetae in gull pellets (Pearson’s chi-squared test with Yates’ correction, ꭕ2=234.99, n=314,
144 P<0.01). Of the 89 pellets in which coarse vegetation made up at least 40% of the bulk of
145 the pellet, 85 (95.5%) had large numbers of earthworm chaetae. Conversely, of the
146 remaining 225 pellets with moderate, little or no coarse terrestrial vegetation, only 13 (5.8%)
147 contained large numbers of earthworm chaetae. Fragments of terrestrial arthropods (mostly
148 beetles of the Order Coleoptera and earwigs of the Order Dermaptera) were found in 73
149 pellets (23.2%), although never comprising 25% of the bulk of any pellet, and there was a
150 highly significant association between the presence of much coarse terrestrial vegetation
151 and the detection of fragments of terrestrial arthropods (Pearson’s chi-squared test with
152 Yates’ correction, ꭕ2=58.54, n=314, P<0.01). These findings support earlier suggestions that
153 terrestrial vegetation had been accidentally picked up with food items (Harris 1965; Vernon
154 1970; Coulson & Coulson 2008). Based on the strong association between terrestrial
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155 vegetation and large numbers of earthworm chaetae, we recommend that, in future studies,
156 pellets with large quantities of coarse terrestrial vegetation be examined for the presence of
157 earthworm chaetae using appropriate methodology.
158 To enhance the detection of earthworm chaetae, we adopted a simple and inexpensive
159 methodology that could be used after minimal training. The technique also detected other
160 structures such as the microscopic remains of food items and the eggs of parasitic
161 helminths, including syngamid roundworms, hairworms and flukes. The trade-off for
162 simplicity was reduced sensitivity. It is highly unlikely that all the earthworm chaetae were
163 initially recovered from each pellet, and subsequent dilution factors further reduced the
164 sensitivity. However, the level of sensitivity was considered acceptable as earthworms
165 typically have eight chaetae for each of their 100-150 segments (Edwards & Bohlen 1996)
166 and thus a single earthworm can have many hundreds of chaetae. Similar or adapted
167 methodology could, therefore, be used in future studies looking at the composition of gull
168 pellets and diets.
169 Coulson & Coulson (2008) found that earthworms frequently contributed to the diet of Lesser
170 Black-backed Gulls breeding in an inland colony in southwest Scotland and recommended
171 that further studies be carried out in other large gulls. Our study has shown that the same is
172 true for Herring Gulls breeding in a coastal colony in southwest Scotland, although they also
173 consumed marine food and other terrestrial items such as cereal and refuse. This may
174 suggest that earthworms can constitute an important part of the Herring Gull’s diet even
175 when other commonly used food resources are available. It adds to our understanding of the
176 diet of Herring Gulls and provides a baseline against which findings from future studies may
177 be compared, should changes in agricultural land use, refuse management or local fishery
178 activity influence resource use by breeding Herring Gulls.
179
180 Acknowledgements
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181 SAC Consulting Veterinary Services, Auchincruive, Ayr, kindly provided access to the
182 Olympus binocular microscope. Roselle Smith, Klaudyna Maniszewska and James Scarlett
183 from Glasgow University assisted in the collection of some of the pellets. We are also
184 grateful to the anonymous reviewer whose comments greatly improved the text.
185
186
187 References
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244
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245 Figure legends
246
247 Figure 1. Earthworm chaeta from gull pellet from Lady Isle. Bar=100 µm.
248
249
250 Figure 2. Much coarse terrestrial vegetation in pellet containing large numbers of earthworm
251 chaetae.
252
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