The effect of cormorants on the plant-arthropod food web on

their nesting islands by

Gundula Kolb

Plants & Ecology Plant Ecology 2009/2

3

Department of Botany Stockholm University The effect of cormorants on the plant-arthropod food web on

their nesting islands

Licentiate thesis by

Gundula Kolb

Supervisors: Peter Hambäck and Lenn Jerling

4

Plants & Ecology

Plant Ecology 2009/2 Department of Botany Stockholm University Plant & Ecology

5

Plant Ecology Department of Botany Stockholm University S-106 91 Stockholm Sweden © Plant Ecology ISSN 1651-9248 Printed by Solna Printcenter Cover: Pictures from an island (Bergskärit) with nesting cormorants in Stockholm’s archipelago. Photo by Svante Jerling.

Abstract

Seabirds have profound effects on plants and animals on their nesting islands by

depositing large amounts of nitrogen and phosphorus rich guano and providing their

living and dead bodies. Most studies on plant communities from seabird affected areas

describe an increased productivity or biomass, except where nutrient loads got toxic due

to very high seabird densities or drought. Several previous studies also have investigated

responses by specific arthropod species and lizards to seabird colonies but our study is

the first to include both plants and all major aboveground arthropod groups. To identify

major pathways in the island food webs, we used the different carbon isotope signals

from terrestrial plants and algae, and the strong nitrogen isotope signal from guano.

Firstly, we found that food web consequences on land also depend on processes in

surrounding water bodies. Major predators on the islands, such as spiders, utilise marine

food items to a high extent, mainly chironomids but to a lesser extent also terrestrial

detritivores feeding on algal detritus on the shore. As a consequence, density changes in

marine invertebrates due to cormorants may affect predator densities on land. Secondly,

decreased vegetation cover and increased plant nutrient content on active cormorant

islands affected three of five investigated herbivore taxa. Lepidopteran larvae and aphids

increased and herbivore beetles decreased on active cormorant islands. The effects on

aphid densities cascaded up to an increased coccinelid density. In contrast to active

6

cormorant islands, abandoned islands had a higher plant biomass than non-bird islands.

The two arthropod groups that seemingly responded to this increased plant biomass were

lepidopterens and web-building spiders. Thirdly, the decreased vegetation cover on active

cormorant islands seemingly has direct negative consequences for some predators, such

as ground living lycosid spiders. This negative effect through vegetation cover might be

one reason why we did not find increased densities of predator on active cormorant

islands despite increased prey (chironomids and brachycerid flies) densities.

Fourthly, also marine algae and invertebrates from the active cormorant islands

surrounding water bodies were affected by the avian nitrogen, but only islands with a

high nest density showed a distinct effect. Marine algae and invertebrates collected

nearby active cormorant islands with a high nest density showed enriched δ15N

signatures. We furthermore found 8-12 times higher densities of two (Iaera albifrons and

chironomids) of the seven investigated invertebrate taxa.

7

Introduction

Fluxes of nutrients, energy and individuals across ecosystem boundaries is ubiquitous,

and can have strong impacts on the dynamics and structure of recipient food webs,

although it is not yet clear how strong the effects of these subsidies are in all systems

(Polis et al. 1997b; Marczak and Richardson 2007) .Theoretical considerations suggest

that the strongest effects should be found in recipient systems with a lower productivity

than the donor system (Polis et al. 1997b), whereas empirical studies suggest that the

importance of the productivity gradient for spatial subsidies can be modified by the

mobility traits of the recipient consumers and their degree of specialization on the

interface habitat (Paetzold et al. 2008). Cross habitat fluxes play an important role in

many coastal ecosystems and occur at several trophic levels (Polis and Hurd 1996a-b;

Polis et al. 2004): shore drift of carrion and detrital algae (Polis and Hurd 1996b, Partzold

et al. 2008), windblown sea foam and spray (Polis et al. 2004), animals (e.g. seabirds)

which feed in the sea but nest and rest on land (e.g.Gillham 1956, 1961; Lindeboom

1984; Polis and Hurd 1995; Sanchez-Pinero and Polis 2000; Barrett et al. 2005) and

emerging aquatic insects (Murakami and Nakano 2002; Sanzone et al. 2003).

Seabirds are represented in great number and play a very important role in coastal

ecosystems both as consumers (Schneider et al. 1987) and as vectors transporting marine

nutrient and organic material to land (Hutchinson 1950; Polis et al. 2004; Ellis et al.

2006). Small islands are often favored by seabirds as nesting and roosting places, due to

the absence of predators (Sanchez-Pinero and Polis 2000). Seabirds deposit large

amounts of N- and P- rich guano on their nesting and roosting islands (Hutchinson 1950;

Lindeboom 1984; Barrett et al. 2005; Wait et al. 2005). Hutchinson (1950) estimated that

104-105 tons of P is annually transferred to land by seabirds. The nutrients from the

guano are incorporated into the soil and increase the concentration of nitrogen and

phosphorus (Smith 1978; Anderson and Polis 1999; Ellis 2005; Ellis et al. 2006)

indirectly affecting plants growing on the islands. It as been shown, that plants growing

in seabird affected areas have enriched N and P concentrations (Anderson and Polis

1999; Ellis 2005; Hobara et al. 2005). Moreover, most studies describe an increased

aboveground plant biomass, or productivity, and a decreased species richness of plants

8

growing in seabird affected areas, except where densities of birds were extremely high or

where precipitation was extremely low (Gillham 1960; Smith 1978; Anderson and Polis

1999; Ellis 2005; Wait et al. 2005). It is also likely that the effect on vegetation depends

on the density, biology and behavior of the nesting bird species (Ellis et al. 2006, Ellis

2005).

Changes in the vegetation due to nutrient input might lead to changes in the density

and diversity of herbivores, detritivores and therefore, indirectly, their natural enemies

(Siemann 1998; Siemann et al. 1998; Pace et al. 1999; Haddad et al. 2000; Zvereva and

Rank 2003; Fonseca et al. 2005; Kagata et al. 2005). An example of such a bottom-up

mechanism caused by the guano deposition of seabirds was described by Barrett et al.

(2005). They found about three times higher lizard densities in coastal areas on seabird

islands as compared to coastal areas on non-bird islands. Stable isotope analysis indicated

that lizards mainly utilised the guano → plant → herbivore pathway. Sanchez-Pinero and

Polis (2000) similarly found that tenebrionid beetles increased on seabird islands in the

Gulf of California but the indirect effects via guano was only apparent in wet years on

roosting islands. The beetle density on nesting islands was more affected via carrion and

fish scraps. The superabundance of scavengers and parasites which convert marine bird

tissue in potential prey explain the extraordinarily high density of spiders found on

seabird islands in the same area (Polis and Hurd 1995). None of the studies on the effect

of seabirds on aboveground consumers on their nesting islands took possible marine feed-

back mechanism into account. Avian nitrogen from the guano may make its way from the

islands into the water, further into marine algae and their consumers. Emerging insects

with aquatic larvae which were feeding on the fertilized algae may enter the islands

providing food for terrestrial consumers. In the Baltic, chironomids, a family with aquatic

larvae, occur in high numbers and play an important role as food source for costal

consumers (Mellbrand et al. in prep). Therefore it might be important to include the

surrounding water bodies in our study system.

9

Aim of this thesis:

Within my study, I will mainly investigate the effect from a dominant seabird on the

structure of arthropod food webs on their nesting islands in the archipelago of Stockholm,

Sweden. Particularly I want to answer the following questions:

1) How do cormorants affect the aboveground plant biomass and the nitrogen content of

plants?

2) How are food webs constructed on islands with and without cormorant nesting

colonies? What are the main prey sources for different predator groups? Do predators

change diet in response to changes in prey availability?

3) How do cormorants affect the density of herbivorous, detritivorous and predatory

arthropods respectively?

In future studies, I will also investigate if the diversity of plants, beetles, bugs, spiders

and there main prey (phantom midges) is affected by cormorant colonies. I will also

examine effects from cormorant colonies on algae and invertebrates in the surrounding

water body.

Material and Methods

Study area

The archipelago of Stockholm, Sweden, consists of about 24 000 islands with sizes

varying between less than one square-meter and several square-kilometers. The

archipelago is subjected to isostatic rebound, currently at a rate of 0.47 cm/year (Ericson

and Wallentinus 1977), which means that the islands are relatively young (Lofgren and

Jerling 2002). The bedrock of study islands consists of granite-gneiss, with a mostly very

thin soil layer. Some islands are partly covered with cliffs and stones. The yearly

precipitation averages 518 mm; the mean temperature is 6.1°C. The highest precipitation

and temperature occur in summer.

The vegetation differs from island to island; some islands are only covered with bare

rocks, others with herbs and grasses or even forests. Bigger islands are built with houses,

mainly summer houses, and partly extensive cultivated. Even small islands have been

10

used by humans for grazing until 50 years ago. Today, islands are visited by tourists for

swimming and sun bathing. For our research, we used seven active and three abandoned

cormorant nesting islands in a subsection of the archipelago, and nine structurally similar,

but neighboring, islands without nesting cormorants (Tab. 1, Fig. 1). The islands differ in

size (0.3-2.7 ha), distance from the mainland (0.1 and 18 km) and vegetation, but we tried

to choose appropriate control islands in relation to the cormorant islands. The nest density

in the active cormorant colonies ranged from 0.007 to 0.063 nest/m² and the time span

since colonization was four to ten years. The cormorant colonies on abandoned islands

have been absences since 2000, 2005 and 2006, respectivly

The dominant tree species are Pinus sylvestris, Alnus glutinosa and Sorbus

aucuparia. Common shrubs are Juniperus communis, Rosa canina and Rubus idaeus. The

most widespread herbs and grasses along the shore are Atriplex spp, Glaux martima,

Filipendula ulmaria, Valeriana salina, Lythrum salicara, Phragmites australis and

Phalaris arundinacea. Tanacetum vulgare, Veronica longifolia, Viola tricolor, Sedum

acre, Sedum telephium and the grasses Festuca pratensis and Deschampsia flexuosa grow

frequently on most islands. On forested islands without cormorant colonies, Anemone

nemorosa, Convallaria majalis, Polygonatum odoratum, Geranium robertianum and

Viola riviniana are common species. On islands with a high nest density in cormorant

colonies high biomasses of Urtica dioica and Galeopsis spp can occur locally. The herb

layer on islands with high nest density is partly missing, especially near or under nests,

exposing the bare soil with a visible detritus layer.

11

Tab. 1: Summary of the 19 study island

area

(m2)

number of active

cormorant nests

Density

(2007)

(nest/m2)

time span of

active

colonization

Stable

isotope

sampling

2005 2006 2007

cormorant

islands

Marskärskobben 7164 81 186 177 0.025 2003-2008 Yes

St.Halmören 8091 222 0 0 0.000 2002-2005 Yes

St.Träskär 15729 80 50 0 0.000 1996-2005 Yes

Kattören 3264 0.000 1997-2000 No

N.Småholmen 8550 410 591 538 0.063 2000-2008 Yes

S.Småholmen 7012 176 194 188 0.027 1998-2008 No

N.Ryssmasterna 3224 65 171 127* 0.040 2003-2008 Yes

S.Ryssmasterna 3687 61 0.017 ?-2008 No

Bergskäret*2 22728 555 595 656 0.029 1998-2008 Yes

Delö*6 1702 37 42 13 0.007 2002-2008 Few

non-cormorant islands

Fårörarna 3286 Yes

Norröra 12475 No

Ägglösen 17357 Yes

V.Mellgrund 3889 Yes

Ljusstaken 5525 No

Hannasholmen 7743 Few

Nickösörarna 5209 Yes

Mjölingsören 27285 Yes

Ostkanten 2337

No

12

A

B C

Fig.1. A: Study area, archipelago of Stockholm, Sweden (°islands with abandoned cormorant colonies • islands with active cormorant colonies, the thick frame includes the study area of the main study, the dashed frame includes the 2nd study area of the aquatic study); B: cormorant nests on the ground; C: cormorant nesting tree.

13

Study species

Cormorants

Great cormorants (Phalarocorax carbo) are one of the best known wild European

seabirds, belonging to the family of cormorants (Phalacrocoracidae) and to the order of

web-footed birds (Pelecaniformes). Three subspecies exist in Europe: Ph. c. carbo on the

Atlantic coast, Ph. c. maroccanus along the coasts of Morocco and Ph. c. sinensis in

south-eastern Europe to China. The latter is the subspecies occuring in the study area.

Great cormorants are opportunistic foragers, but usually prefer small fish, either small

species or young individuals from larger species. They are good divers and hunt under

water usually to depths of 2-6 m. Cormorants breed and roosts in trees, on bare soil or

rocks and in reed beds (Fig. 1). They live in colonies of up to 10000 pairs (nesting

colonies) or 12000 individuals (roosts) (Carss 2002).

Great cormorants (Ph. c. sinensis) in Sweden have a long history; 8000-13000 years

old bones have been found. During the 19th century cormorant colonies existed in the

south of Sweden (Skåne and Blekinge), but they disappeared in the beginning of the 20th

century. They started to re-colonize the south of Sweden (Kalmarsund) in 1948. The

archipelago of Stockholm was recolonized in 1994. Their abundance in the Stockholms

archipelago had increased to 5759 pairs in 21 colonies by 2007 (Staav 2007). The

colonies are active between April and August and span between 4 and 776 pairs in the

area. During fall, birds migrate and overwinter in the Mediterranean and in the Black Sea.

Cormorants are disliked in Sweden, despite those cormorants have a long history in

Sweden and that their presence has a positive effect on threatened birds, like sea eagles

and guillemots, by providing prey and creating favored nesting habitats. Cormorants are

blamed by fishermen for reduced catches and by the public for damaging the

environment. Despite the controversial public discussion and the increasing cormorant

density in Europe not much scientific research have been done on the impact of

cormorant colonies on insular ecosystems.

14

Arthropods

In this study, I focused on aboveground arthropods. Arthropods living on islands are

either purely terrestrial taxa or emerging insects with aquatic larvae. Phantom midges

(Chironomidae) are by far the most abundant family with aquatic larvae. A study by

Mellbrand and Hambäck (unpubl.) has shown that chironomids play an important role as

prey items, especially for spiders, in costal food webs of the Baltic Sea. The most

abundant predators are wolfspiders (Lycosidae), web-building spiders (Linyphiidae,

Araneidae and Tetraganthidae), damsel bugs (Nabidae), ground beetles (Carabidae), rove

beetles (Staphylinidae) and ladybird beetles (Coccinelidae). Common herbivores are

butterfly larvae (Lepidoptera), aphids (Aphididae), cicadas (Homoptera) and beetles

(Chrysomelidae, Curculionidae). Widely distributed detritivores are brachycerid flies

(Diptera) and woodlice (Isopoda).

Methods

Stable isotope analysis

Stable isotope analysis has become a popular tool for ecologists to elucidate the structure

of food webs, to calculate the importance of marine food versus terrestrial food sources

for terrestrial consumers and to trace the fate of avian nitrogen (Lindeboom 1984;

Anderson and Polis 1998; Wainright et al. 1998; Barrett et al. 2005; Paetzold et al.

2008). Consumers typically reflect the stable isotope composition of their food source

with some predictable changes (fractionation). In general, carbon isotope ratios change

only little between trophic levels, whereas the nitrogen isotope ratios show more distinct

increases (McCutchan et al. 2003; Vanderklift and Ponsard 2003). Carbon isotope ratios

are clearly separated between marine and terrestrial plants, whereas nitrogen isotope

ratios show a much larger variability. Carbon isotope ratios are therefore an often more

predictable source for identifying the relative importance of marine and terrestrial carbon

for consumers (Barrett et al. 2005). Fish-eating cormorants have, however, according to

their relatively high trophic position strongly elevated δ15N values (Barrett et a.l 2005).

This difference is further enhanced through the fast mineralization of uric acid to

ammonium (NH4), a chemical reaction that selectively removes 14N from guano

15

(Lindeboom 1984; Wainright et al. 1998). This isotope enrichment also translates into

enriched δ15N signatures of soils, plants and their consumers in cormorant effected areas

(Barrett et al. 2005). Stable isotope values of nitrogen can therefore be used to trace the

fate of avian nitrogen on and around islands. In this study, I used stable isotope analysis

to delimit the food web structures on island on the different island types and trace the fate

of marine N and C. Based on the δ13C and δ15N, I estimated the relative proportion of

marine and terrestrial carbon and nitrogen in higher trophic level with help of mixing

models (Phillips and Gregg 2001). These calculations also benefited from the fact that

even though marine algae and their consumers around the islands might be enriched in 15N from guano on islands, the carbon isotope ratios have distinct marine signatures.

Based on the results of the stable isotope analysis and mixing model, we constructed food

webs of the islands and examined differences in the food web due to cormorant colonies.

Sampling

Vegetation cover and aboveground biomass were estimated in July 2007. Arthropod

densities were estimated in August 2007 by sampling ten points on each island, using a

converted leaf blower. The samples were identified to species, family or order level

(depending on taxa) and weighed.

Specimens from the D-Vac sampling were complemented with hand collection,

sweep netting and pit-fall traps in July and August 2006-2008, to collect samples for

stable isotope analyses. Stable isotope sampling was mainly done on 11 study islands

with some additional samples from remaining study islands in at least three plots per

islands. Samples from six terrestrial plant species, brown macro algae (Fucus

vesiculosus), its epiphytic algae and 20 terrestrial arthropods taxa from different trophic

levels were analyzed.

16

Result and discussion

Seabirds certainly have profound effects on plant and animals on their nesting islands, by

depositing large amounts of nitrogen and phosphorus rich guano and providing their

living and dead bodies (e.g. Gillham 1956; Duffy 1983, Polis and Hurd 1995; Anderson

and Polis 1999; Polis et al. 2004; Sanchez-Pinero and Polis 2000; Barrett et al. 2005;

Wait et al. 2005; Ellis 2005). Most studies on plant communities from seabird affected

areas describe an increased productivity or biomass, except where nutrient loads got toxic

due to very high seabird densities or drought ( Smith 1976; Anderson and Polis 1999;

Sanchez-Pinero and Polis 2000; Wait et al. 2005; Ellis 2005). Several previous studies

have investigated responses by specific arthropod species and lizards to seabird colonies

(Polis and Hurd 1995; Sanchez-Pinero and Polis 2000; Barrett et al. 2005) but our study

is the first to include both plants and all major aboveground arthropod groups. First, we

were able to use the carbon isotope signal from terrestrial plants and algae, and the

nitrogen isotope signal from guano to identify major pathways in the island food webs

and construct a preliminary food web (Fig, 2 and 3).

-6

-4

-2

0

2

4

6

-32 -30 -28 -26 -24 -22 -20 -18

-6

-4

-2

0

2

4

6

-32 -30 -28 -26 -24 -22 -20 -18

Ants

Collembola

Flies

Isopoda

Carabidae

Coccinellidae

Nabidae

Saldidae

Staphylinidae

Lycosidae

web-spiders

Heteroptera

Cicadina

Lepidoptera

Aphids

Green algae

Chironomids

Trichoptera

Terrestrial plants

Algae

Herbivores

Marine prey

Insect preds

Spiders

Detritivores

δ13C (‰)

stan

dard

izedδ

15N

(‰

)

Fig. 2: Biplot with 13C and standardized 15N for all major taxa on islands (mean±S.E.). 15N has been standardised at an island level by correcting for the mean isotope ratio of those taxa that occurred on all island. For instance, 15N(Nabidae)standardised=15N(Nabidae)raw -

15Nmean for island. This standardisation essentially removes the cormorant effect and facilitates an examination of food web effects.

17

Cormorants

Fish

Algae

soil food web

Flies Collembola

Detrivores

Isopoda

•Linyphiidae

•Araneidae

•Tetragnathidae

Lycosidae

Carabidae

Nabidae

Saldidae

Staphylinidae

Parasites Scavengers

Beetles Flies

Herbivores

Plants

Guano

Chironomidae

Coccinelidae

Formicidae

Fig. 3: Preliminary arthropod food web on islands with active cormorant colonies in the archipelago of Stockholm, Sweden. Black lines = mainly signal of marine carbon (enriched δ13C signature) and avian nitrogen (enriched δ15N signature), dashed lines = mainly signature of avian nitrogen (enriched δ15N signature). The size of the line represents the strength of the signal. The thicker the line the stronger is the signal.

Most interestingly, we show that in order to understand food web consequences on

land it is necessary to include also surrounding water bodies. Major predators on the

islands, such as spiders, utilise marine food items to a high extent, mainly chironomids

but to a lesser extent also terrestrial detritivores (flies) feeding on algal detritus on the

shore. Furthermore, some taxa seemed to changed diet between islands with and without

cormorant colonies. Five taxonomic groups (Chilopoda, Nabidae, Linyphiidae, Araneidae

and Pachygnatha) had a higher relative consumption of marine prey on islands with

18

abandoned cormorant colonies, and two other taxonomic groups (Saldidae and

Staphylinidae) had a higher relative consumption of marine prey on islands with active

colonies (Fig. 4). Second, our data suggest that the decreased vegetation cover on islands

with active cormorant colonies has direct negative consequences for some predators, such

as ground living lycosid spiders.

0

0.2

0.4

0.6

0.8

1

1.2

Lin

yph

iida

e

Ara

ne

ida

e

Te

tra

gn

ath

a

Lyc

osi

da

e

Pa

chyg

na

tha

Ca

rab

ida

e

Sta

ph

ylin

ida

e

Na

bid

ae

Sa

ldid

ae

Ch

ilop

od

a

Co

ccin

elid

ae

an

ts

Flie

s

Iso

po

da

Co

llem

bo

la

% m

arin

e C

sou

rce

control island

abandoned cormorant island

active cormorant island

Fig.4. Proportion marine and terrestrial carbon in the diet of the main arthropod predator and detritivores groups based on two-source diet mixing models with marine epiphytic algae and terrestrial plants as baseline on island with active or abandoned cormorant colonies and on islands without seabird colonies in the archipelago of Stockholm, Sweden (means±SE).

Our study showed that cormorants strongly affect the vegetation on their nesting

islands. We found up to 80% decreases in vegetation cover and 1.6-2.7 times higher plant

nitrogen content on active cormorant islands, whereas the aboveground plant biomass

were only effected on abandoned islands. On abandoned islands the plant biomass was

2.4 times higher than on control islands. Such changes in the quantity and quality of plant

biomass are expected to affect consumers at higher trophic levels (Hunter and Price 1992;

Siemann 1998; Siemann et al. 1998; Pace et al. 1999; Haddad et al. 2000; Fonseca et al.

2005; Zvereva and Rank 2003; Kagata et al. 2005), and this was to some extent also

observed in our study. Aphids and butterfly larvae seem mainly to profit from the

increased nitrogen content, as they showed the highest densities and the highest weights

19

on active cormorant islands. In contrast, herbivorous beetles seem to suffer from the

lower vegetation cover on these islands. On abandoned islands lepidopteren larvae

seemed to profit from increased plant biomass, with a higher density on this island

category than on control islands (Fig.5).

We also expected detritivores – as reported by Sanchez-Pinero and Polis (2000) – to

respond to cormorant colonies. Detritivores can be affected by seabirds in two separate

ways, either directly through the consumption of seabird carcasses and by-products or

indirectly through the observed changes in the vegetation. In our study, only brachycerid

flies responded to cormorants, and they had an about five times higher density on active

cormorant islands than on islands without current colonies. The isotope data further

suggest that this increased density was mainly caused by a direct effect of cormorants and

not via the vegetation. Diptera is an extremely species rich family, including both bird

parasites and scavengers, so it is very likely that islands with nesting cormorants included

species not present on other islands. Another detritivorous taxa, isopods, had also highly

enriched δ15N signatures on active colonies, but isopods did not show any density

response to cormorants. The lack of density response of detritivores, other than flies,

might be explained by their use of other abundant detritivorous material, such as shore-

drifted algae and terrestrial plants.

Shore-line predators also use aquatic prey sources beside terrestrial food sources

(Murakami and Nakano 2002; Sanzone et al. 2003). To study and explain the effect of

nesting cormorants on predators, we therefore first had to understand predator-prey

relationships and how prey availability was affected by cormorant colonies. The diet

mixing models, and the related changes in δ13C and δ15N in response to cormorants,

suggest that all investigated web-building spiders mainly prey on chironomids. The

density of chironomids was only affected by nesting cormorants on active islands with a

high nest density, where the chironomids showed an increased density. Web-building

spiders, however, did not show an increased density on active cormorant islands. This

lack of positive density response was even more unexpected, considering the high

brachycerid fly density on these islands. The highest density of web-spiders was instead

found on abandoned cormorant islands where they fed, according to the diet mixing

model and their δ15N signature, mainly on chironomids. This behaviour can neither be

20

explained by the density of chironomids nor by their nitrogen content; which did not

differ among islands. However, web-building spiders on abandoned cormorant islands

might profit from increased lepidoteren density and increased habitat quality, through

increased plant biomass. The ground-living lycosid spiders differ in their ecology and

hunting method from web-building spiders. These differences are reflected in their

response to nesting cormorants. Lycosids seemingly prey, according to the diet mixing

models and to the higher δ15N signature on abandoned and active cormorant islands, to a

lower degree on chironomids. Their δ15N signature on islands with a high nest density is

similar to the δ15N signature of the sarcophagus beetle Omosita colon. This similarity

indicates that lycosids mainly feed on prey that in turn feed directly on cormorants, like

scavengers or parasites, possibly flies. Despite this diet and the high prey abundance on

active cormorant islands, lycosid spiders decreased in density on these islands. The most

likely hypothesis is that lycosids responded strongly to the decreased habitat quality

within colonies, through the reduction in vegetation cover.

Only one group of predatory insects, aphidopagous species, responded significantly

to cormorant colonies. Similar to aphids, their main prey, aphidophagous species showed

the highest density on active cormorant islands. Even though other predatory insect

families did not show numerical responses to cormorant colonies, some families

seemingly changed their diet under the effect of cormorant colonies. The diet mixing

models indicate that nabid bugs, like web-building spiders, increased their feeding of

marine prey (likely chironomids) on abandoned cormorant islands. Saldid bugs similarly

had only marine carbon in their diet on active cormorant islands. The δ15N value of saldid

bugs was however similar to that of lycosids, and could again indicate feeding on prey

that feed directly on cormorant remnants. Also staphylinids and chilopods seemed,

according to their δ15N, to feed on such prey. The lack of positive density response of

main predators in response to increased prey densities on active cormorant islands might

be explained by a lack of food limitation due to constantly high abundances of

chironomids and detritivores. Carabid beetles were beside coccinelids the predatory

family which fed to the highest degree on terrestrial prey, which is reflected in their

isotopic signature intermediate between herbivores and collembolans. The dominant

carabid on islands is Dyschirius globosus, which is known to feed on collembolans and

21

other small ground-dwelling prey.

In our aim to investigate and illuminate the effect of nesting cormorants on the

arthropod food web of their nesting islands, we faced several problems. First, we did not

have explicit information about the trophic fractionation of δ13C and especially δ15N of

the invested consumers. The trophic fractionation of δ15N is seen to vary strongly

between species, within a single species, and among diets (Wolf et al. 2009). The

fractionation of δ13C is known to be smaller than of δ15N but also to vary less between

different species (McCutachan et al. 2003). To be able to calculated reliable predictions

about the diet composition of consumers with the help off three-source-linear models

(Phillips and Gregg 2001), it is therefore necessary to know the actual fractionation of the

investigated species in connection with their diet. Caut et al. (2008), found that diet

mixing models work best when they used fractionation factors estimated experimentally.

Second, food webs on islands are extremely complex and our preliminary food web is

extremely simplified. For example, behind our group brachycerid flies are hidden high

numbers of species belonging to different families with different biology. Some species

are detritivores, some herbivores, some saprophagous, some predators and some

parasites. To separate these groups from each other necessitates further sampling,

determination and stable isotope analysis. We furthermore did not study the soil food

web which is extremely complex and tightly linked to the aboveground food web. For

example, the high δ15N signature of ground living predators on active cormorant islands

might be a result of an enrichment of avian δ15N along members of the soil food web.

Therefore, further studies with other sampling methods, including soil processes and

communities would be needed to complement the information from food web study.

22

0.5

1.0

2.0

Lycosidae

20.00.1 0.2 0.5 1.0 2.0 5.0 10.0 20.0

Distance to mainland (km) (scale is logged)

Density (ind/0.7m²) (scale is logged)

12

105

Web-building spiders

20.00.1 0.2 0.5 1.0 2.0 5.0 10.0 20.0

Distance to mainland (km) (scale is logged)

20.00.1 0.2 0.5 1.0 2.0 5.0 10.0 20.0

Distance to mainland (km) (scale is logged)

0.8

1.0

1.2

1 .4

1.6

1.8

. 60

Parasitic hymenoptera

12

510

20

20.00.1 0.2 0.5 1.0 2.0 5.0 10.0 20.0

Distance to mainland (km) (scale is logged)

Density (ind/0.7m²) (scale is logged)

Brachycerid flies

0. 5

1.0

2.0

5.0

2000 5000 10000 20000

Island area (m²) (scale is logged)

Lepidoptera larvaeSaprophagous beetles

0.5

1.0

1.5

2 .0

2.5

3.5

2000 5000 10000 20000

Island area (m²) (scale is logged)

10

. 0

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

0.5

01

.01

.02

.02

.05

.05

.01

0. 0

Aphidophaga

12

51

01

25

10

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

Density (ind/0.7m²) (scale is logged)

Herbivore beetles Aphids

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

0.5

01

.01

.02

.02

.05

.05

.01

0. 0

10

. 00

.00

.05

05

00

20

0

Fungivore beetles

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

non-bird islandabandoned cormorant islandactive cormorant island

0.5

1.0

2.0

5.0

10

.02

0.0

50

.0

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

Density (ind/0.7m²) (scale is logged)

0.5

1.0

1.5

3.0

2.5

2.0

0.5

1.5

2.0

Chironomidae

me

an d

ensi

ty p

er 0

.7m

2 ve

ge

tate

d a

rea

(sca

le is

log

ged)

m

ean

den

sity

per

0.7

m2

ve

ge

tate

d a

rea

(sca

le is

log

ged)

m

ean

de

nsity

per

0.7

m2

ve

geta

ted

are

a (s

cale

is lo

gged

) m

ean

de

nsity

per

0.7

m2

ve

geta

ted

are

a (s

cale

is lo

gged

)

Fig. 7: Mean arthropod density per 0.7m2 vegetated island on non-seabird islands (=control islands), on islands with abandoned colonies and on island with active cormorant colonies in the archipelago of Stockholm, Sweden.

23

Further studies

Diversity

Several studies have shown that plant diversity decreases with an increasing nutrient load

(Huston 1994; Siemann 1998). According to this general trend seabird islands often

harbour a lower plant species number than islands without seabirds (Ishida 1996, Wait et

al. 2005). A decreased plant diversity is further assumed to lead to a decrease in

herbivore diversity (Hutchinson 1959; Tilman 1982; Siemann 1998). We therefore

expected lower plant and herbivore diversity on active cormorant nesting islands with

high nest densities. On the other hand, we expected a larger diversity of spiders on

islands with active cormorant colonies than on control islands because of a broader range

of prey items; seabird parasites and scavengers may be abundant on seabird islands and

chironomid densities may be higher on islands with high nest densities.

This study examined the effect of cormorants on the diversity of plants, beetles,

bugs, spiders and chironomids. Sampling and data collection took place between spring

and fall 2007 and during summer 2008. Plant and insect diversity was investigated on the

same islands as density estimates, while spider sampling took place on a subset of these

islands. When examining diversity responses, islands were divided in four categories:

non-bird islands, islands with abandoned cormorant colonies, islands with active

cormorant colonies at a low (< 0.04 webs/m²) or a high (> 0.04 webs/m²) nest density.

The total number of plant species per island was recorded, and the percentage cover in 20

plots (1m x 1m), randomly placed along a 60 m long transect. Beetles and bugs were

collected by D-vacing. Spiders and chironomids were collected by Caroline Essenberg as

a part of her exam work. Ground living spiders were caught in pit fall traps in early July,

spiders sitting in vegetation and chironomids with sweep netting in August. Insects were

stored frozen, and spiders in ethanol, until identification. All imagoes were determined to

species, juveniles and larvae to genus or family level. For the chrironomids only male

individuals were determined.

There was on average of 56±4 plant species on islands without cormorant

colonies, 47±7 species on islands with abandoned cormorant colonies, 46±5 species on

24

active cormorant islands with a low nest density and 36±10 on active cormorant islands

with a high nest density. As expected, nesting cormorant seems to have negative effects

on species diversity; but preliminary analyses indicate that this trend is not statistically

significant. The herb layer on cormorant islands with high nest densities is nevertheless

dominated by only few species.

Sampling of beetles resulted in a total of 1 256 individuals belonging to 149

species and 25 families. Almost 89% of all species belonged to only five families:

weevils (Curculionidae), leaf beetle (Chrysomelidae), rove beetles (Staphylinidae),

ground beetles (Carabidae) and ladybird beetles (Coccinelidae). The categorisation of

beetles into trophic groups resulted in five groups: predators, herbivores, fungivores,

detritivores and saprophagous beetles. The group with the highest number of species and

individuals was herbivores with 65 species, followed by predators with 57 species and

fungivores with 20 species. Detritivores and saprophages were species poor with only 3

and 4 species. Sampling of bugs resulted in a total of 632 individuals belonging to 55

species and 10 families (74 % of the collected bug species were herbivores 26 %

predators). Seed bugs (Lygaeidae) and plant bugs (Miridae) were the two groups with the

highest number of species (64 %) and individuals (77 %). Damsel bugs (Nabidae) were

the only abundance predatory bug family; seven species and 10% of collected bug

individuals. Pitfall sampling of spiders resulted in a total of 1919 indivudals belonging to

40 species and 11 families. The most common genus was Pardosa (Lycosidae), and the

most common species was Pardosa agricola. Sweep web sampling of spiders resulted in

a total of 382 individuals belonging to nine families and 23 species. Tetragnathidae were

the species and individual riches family. About male 8500 chironomids belonging to 43

species were caught.

Total species number of heteropterans and coleopterans did not differ between the

four island categories but showed a trend towards the highest species numbers on islands

with abandoned cormorant colonies. Among the five most common beetle families, only

ladybird beetles showed a significant response to the presence of cormorants; they had

the highest species numbers on active cormorant islands with a low nest density. This

can be explained with high aphid densities on active cormorant islands (see main study).

Leaf beetles and weevils showed a trend towards lowest species numbers on active

25

cormorant islands with a high nest density. This pattern was also supported by a

comparison of the mean number of herbivore beetles per island category; islands with a

high cormorant nest density had the lowest species number while abandoned cormorant

islands had the highest species number. This pattern can be easily explained by the high

aboveground biomass on abandoned cormorant islands and the low vegetation cover and

diversity on active cormorant islands with a high nest density. Fungivorous beetles

showed the highest species numbers on island with abandoned colonies and on active

cormorant islands with a low nest density. Saprophagous beetles were mainly found on

islands with active cormorant colonies. Neither the species number of seed bugs nor the

species number of plant bugs was affected by cormorant colonies. Herbivore and predator

bug species were also not significantly affected by cormorants but showed a similar trend

as the beetle species towards the highest numbers of species on islands with abandoned

cormorant colonies (Fig. 5). The data for spiders and chironomids have not yet been

analysed.

0

5

10

15

20

25

30

Scavengers Detritivores Fungivores Herbivores Predators Coleoptera(total)

0

10

20

30

40

50

60

70

terr. plants

mea

n sp

ecie

s nu

mbe

r

0

2

4

6

8

10

12

14

Heteroptera(total)

Lygaeidae Miridae Nabidae

mean s

peci

es

num

ber

non-bird islands

abandoned cormorant islands

active cormorant islands withlow nest density

active cormorant islands withhigh nest density

Coleoptera

Heteroptera

Fig.5: The mean numbers of beetle species per island on non-seabird islands, on islands with abandoned cormorant colonies and on islands with active cormorant colonies with either a low (<0.04 nests/m2) or a high (>0.04 nests/m2) nest density in the archipelago of Stockholm.

26

Aquatic system

My results show that in order to understand food web dynamics of islands, it is necessary

to include subsidies from the neighbouring water body. The enriched δ15N signatures of

the chironomids on active seabird islands (see main study) indicates that avian nitrogen

from the guano made its way from the islands into the water, further into marine algae

and their consumers. Cormorants also affected the density of adult chironomids, but only

on islands with a high cormorant nest density. The lack of effect from cormorants with

low nest density on the density of chironomid can possibly be explained by the lower

guano load on islands with a low nest density. The isotope analysis suggests that little

nitrogen leak into the water on these islands, presumably because the vegetation on the

island manages to absorb most of the avian nitrogen. The focus for this study was to

examine epiphytic algal and invertebrate responses in waters surrounding islands with or

without cormorant colonies. Former studies have shown that big amounts of nitrogen

from the guano are flushed into the sea and enter the marine food web via aquatic

primary consumers (Lindeboom 1984; Wainright et al. 1998). Wainright et al. (1998)

found that marine primary producers collected near seabird colonies were ca. 6.6‰

enriched in both 15N and 13C compared with those collected elsewhere the shore. While

this study indicated that primary producers get affected by the nutrient input from seabird

colonies, it did not investigate effects on algal productivity. Furthermore, to my

knowledge, no previous study has investigated the effects of seabird colonies on

invertebrates in the surrounding water body. With my study I wanted investigate how the

density and composition of invertebrates living on brown macro algae (Fucus

vesiculosus) nearby islands gets affected by the presents of the cormorant colony.

Brown macro algae (Fucus vesiculosus) were collected in summer 2007 by Janna

Ekholm as a part of her exam work nearby islands in the northern part of the archipelago

of Stockholm, around a subset of the islands of the main study. Samples were taken

nearby seven islands with an active cormorant colony, five with a low (<0.04 nests/m²)

and two with a high (>0.4 nests/m²) nest density, two with an abandoned cormorant

colony and nine without cormorant colonies. In summer 2008, I performed additional

sampling in the southern part of the archipelago of Stockholm nearby four active

cormorant islands with a high nest density and four non-bird islands. Six random samples

27

were taken per island, three samples each on two Fucus fronds. We collected the algae

with the help of fine web bags, in order to sample all invertebrates living on the plants.

Algal samples were frozen until further processing. The epiphytic algae were removed

and the Fucus fronds and the epiphytic algae were weighed separately. All invertebrates

were sorted and counted. The load of epiphytic algae was calculated as the mass (g)

epiphytic algae per gram macro algae. Seven invertebrate taxa (Mollusca: Theodoxus

fluviatilis, Radix baltica and Potamopyrgus; Crustacea: Gammarus spp., Idotea spp,

Iaera albifrons and insecta: Chironomidae) were identified, dried and weighed. The

sampled Fucus plants differed much in size and weight regardless of island category. To

compare invertebrate densities between island categories, we therefore calculated the

number of individuals per unit weight of algae. Per islands, up to five samples from five

taxa (Theodoxus fluviatilis, Gammarus spp., Idotea spp, Iaera spp., Chironomidae) were

used for stable isotope analysis. Preparation and analysis of the stable isotope samples

were performed in similar way as in the main study.

The data analysis of is not yet completed; I have only examined data from 2007. The

stable isotope analysis (Fig. 6) show that the δ15N values of Fucus and epiphytic algae

collected nearby cormorant island with nest densities over 0.04 nests per m² were 3

respectively 5 times higher than the δ15N values of algae collected nearby islands without

colonies. Algae growing nearby cormorant islands with a lower nest density show only a

trend of δ15N enrichment. δ15N from algae growing nearby islands with an abandoned

colony were about equal to the δ15N values of algae growing nearby control islands. The

same pattern was found for the investigated invertebrates, the δ15N signature of all

invertebrates collected nearby islands with an abandoned colony were about equal to the

signatures from control islands. All sampled invertebrate families showed between 2.5 to

5 times higher δ15N values than animals nearby control islands. The δ15N values of

invertebrates collected nearby islands with an active cormorant colony with a low nest

density were between the values from control islands and islands with a high nest density,

but did mostly not differ from control islands. Only Theodoxus and Idotea showed

marginal significant δ15N enrichments compared to control islands.

28

0

4

8

12

16

20

-20 -15 -10

δC (‰)

δC

N (‰

)non-bird island

abandoned cormorantisland

active cormorant islandwith a low nest density

active cormorant islandwith a high nest density

Fucus

epi

chi

cru

mol

Fig. 6: The relationship between δ15N and δ13C values for algae and invertebrates nearby island with abandoned and active cormorant colonies with a low (<0.4 nests/m²) and a high (>0.4 nests/m²) nest density and islands without seabird colonies in the archipelago of Stockholm, Sweden. chi=Chironomidae, cru=Crustacea (Gammarus spp., Idotea spp, Iaera albifron), epi=epiphytic algae, mol=Molluca (Theodoxus fluviatilis)

Only two invertebrate taxa changed in abundance between island categories (Fig. 7). We

found 12 times more chironomid larvae and 8 times more Iaera albifrons in Fucus

samples collected nearby islands with a high nest density (>0.05 nests per m²) than in

Fucus plants collected nearby islands without a cormorant colony. No taxa showed

density responses to abandoned colonies or colonies with a low nest density.

The proportional weight of epiphytic to Fucus algae was about equal for all island

categories. Our study shows that only cormorant colonies with extremely high nest

density affect the marine primary producers and consumers. Further studies are needed to

investigate in which radius around the islands an effect on marine primary producers and

consumers is detectable.

29

0

24

68

10

1214

16

Theodo

xus

Gamm

arus

Idot

ea

Chriono

midae

Iaer

amea

n nu

mbe

r of

ind

per

gram

dr

y-w

eigh

t al

gae non-bird islands

abandoned cormorantislands

active cormorant islands withlow nest density

active cormorant islands withhigh nest density

Fig. 7: The mean number of invertebrates per gram dry-weight Fucus between non-seabird islands, islands with abandoned cormorant colonies and islands with active cormorant colonies with a low (<0.04 nests/m2) and a high (>0.04 nests/m2) nest density in the archipelago of Stockholm.

Acknowledgement

Thanks to Peter Hambäck and Lenn Jerling for supervision, to Janna Ekholm and

Caroline Essenberg for providing data from their exam works, to Hanna Axemar, Annika

Lindström, Maria Enskog, Svante Jerling, Eskil Jerling and Bitte Jerling for helping in

the field and lab and to Hans-Erik Wanntrop and Carl-Cedric Coulianos for determine

beetles and bugs.

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beetle Chrysomela lapponica. - Oecologia 135(2): 258-267.

34

Serien Plants & Ecology (ISSN 1651-9248) har tidigare haft namnen "Meddelanden från Växtekologiska avdelningen, Botaniska institutionen, Stockholms Universitet" nummer 1978:1 – 1993:1 samt "Växtekologi". (ISSN 1400-9501) nummer 1994:1 – 2003:3.

Följande publikationer ingår i utgivningen: 1978:1 Liljelund, Lars-Erik: Kompendium i matematik för ekologer. 1978:2 Carlsson, Lars: Vegetationen på Littejåkkadeltat vid Sitasjaure, Lule

Lappmark. 1978:3 Tapper, Per-Göran: Den maritima lövskogen i Stockholms skärgård. 1978:4: Forsse, Erik: Vegetationskartans användbarhet vid detaljplanering av

fritidsbebyggelse. 1978:5 Bråvander, Lars-Gunnar och Engelmark, Thorbjörn: Botaniska studier vid

Porjusselets och St. Lulevattens stränder i samband med regleringen 1974. 1979:1 Engström, Peter: Tillväxt, sulfatupptag och omsättning av cellmaterial hos

pelagiska saltvattensbakterier. 1979:2 Eriksson, Sonja: Vegetationsutvecklingen i Husby-Långhundra de senaste

tvåhundra åren. 1979:3 Bråvander, Lars-Gunnar: Vegetation och flora i övre Teusadalen och vid

Auta- och Sitjasjaure; Norra Lule Lappmark. En översiktlig inventering med anledning av områdets exploatering för vattenkraftsändamål i Ritsemprojektet.

1979:4 Liljelund, Lars-Erik, Emanuelsson, Urban, Florgård, C. och Hofman-Bang, Vilhelm: Kunskapsöversikt och forskningsbehov rörande mekanisk påverkan på mark och vegetation.

1979:5 Reinhard, Ylva: Avloppsinfiltration - ett försök till konsekvensbeskrivning. 1980:1 Telenius, Anders och Torstensson, Peter: Populationsstudie på Spergularia

marina och Spergularia media. I Frödimorfism och reproduktion. 1980:2 Hilding, Tuija: Populationsstudier på Spergularia marina och Spergularia

media. II Resursallokering och mortalitet.

1980:3 Eriksson, Ove: Reproduktion och vegetativ spridning hos Potentilla anserina L. 1981:1 Eriksson, Torsten: Aspekter på färgvariation hos Dactylorhiza sambucina. 1983:1 Blom, Göran: Undersökningar av lertäkter i Färentuna, Ekerö kommun. 1984:1 Jerling, Ingemar: Kalkning som motåtgärd till försurningen och dess effekter

på blåbär, Vaccinium myrtillus. 1986:1 Svanberg, Kerstin: En studie av grusbräckans (Saxifraga tridactylites)

demografi. 1986:2 Nyberg, Hans: Förändringar i träd- och buskskiktets sammansättning i

ädellövskogen på Tullgarnsnäset 1960-1983. 1987:1 Edenholm, Krister: Undersökningar av vegetationspåverkan av vildsvinsbök i

Tullgarnsområdet. 1987:2 Nilsson, Thomas: Variation i fröstorlek och tillväxthastighet inom släktet

Veronica. 1988:1 Ehrlén, Johan: Fröproduktion hos vårärt (Lathyrus vernus L.). - Begränsningar

och reglering.

35

1988:2 Dinnétz, Patrik: Local variation in degree of gynodioecy and protogyny in Plantago maritima.

1988:3 Blom, Göran och Wincent, Helena: Effekter of kalkning på ängsvegetation. 1989:1 Eriksson, Pia: Täthetsreglering i Littoralvegetation. 1989:2 Kalvas, Arja: Jämförande studier av Fucus-populationer från Östersjön och

västkusten. 1990:1 Kiviniemi, Katariina: Groddplantsetablering och spridning hos smultron,

Fragaria vesca. 1990:2 Idestam-Almquist, Jerker: Transplantationsförsök med Borstnate. 1992:1 Malm, Torleif: Allokemisk påverkan från mucus hos åtta bruna makroalger på

epifytiska alger. 1992:2 Pontis, Cristina: Om groddknoppar och tandrötter. Funderingar kring en klonal

växt: Dentaria bulbifera. 1992:3 Agartz, Susanne: Optimal utkorsning hos Primula farinosa. 1992:4 Berglund, Anita: Ekologiska effekter av en parasitsvamp - Uromyces lineolatus

på Glaux maritima (Strandkrypa). 1992:5 Ehn, Maria: Distribution and tetrasporophytes in populations of Chondrus

crispus Stackhouse (Gigartinaceae, Rhodophyta) on the west coast of Sweden. 1992:6 Peterson, Torbjörn: Mollusc herbivory. 1993:1 Klásterská-Hedenberg, Martina: The influence of pH, N:P ratio and

zooplankton on the phytoplanctic composition in hypertrophic ponds in the Trebon-region, Czech Republic.

1994:1 Fröborg, Heléne: Pollination and seed set in Vaccinium and Andromeda. 1994:2 Eriksson, Åsa: Makrofossilanalys av förekomst och populationsdynamik hos

Najas flexilis i Sörmland. 1994:3 Klee, Irene: Effekter av kvävetillförsel på 6 vanliga arter i gran- och tallskog. 1995:1 Holm, Martin: Beståndshistorik - vad 492 träd på Fagerön i Uppland kan

berätta. 1995:2 Löfgren, Anders: Distribution patterns and population structure of an

economically important Amazon palm, Jessenia bataua (Mart.) Burret ssp. bataua in Bolivia.

1995:3 Norberg, Ylva: Morphological variation in the reduced, free floating Fucus vesiculosus, in the Baltic Proper.

1995:4 Hylander, Kristoffer & Hylander, Eva: Mount Zuquala - an upland forest of Ethiopia. Floristic inventory and analysis of the state of conservation.

1996:1 Eriksson, Åsa: Plant species composition and diversity in semi-natural grasslands - with special emphasis on effects of mycorrhiza.

1996:2 Kalvas, Arja: Morphological variation and reproduction in Fucus vesiculosus L. populations.

1996:3 Andersson, Regina: Fågelspridda frukter kemiska och morfologiska egenskaper i relation till fåglarnas val av frukter.

1996:4 Lindgren, Åsa: Restpopulationer, nykolonisation och diversitet hos växter i naturbetesmarker i sörmländsk skogsbygd.

1996:5 Kiviniemi, Katariina: The ecological and evolutionary significance of the early life cycle stages in plants, with special emphasis on seed dispersal.

1996:7 Franzén, Daniel: Fältskiktsförändringar i ädellövskog på Fagerön, Uppland,

36

beroende på igenväxning av gran och skogsavverkning. 1997:1 Wicksell, Maria: Flowering synchronization in the Ericaceae and the

Empetraceae. 1997:2 Bolmgren, Kjell: A study of asynchrony in phenology - with a little help from

Frangula alnus. 1997:3 Kiviniemi, Katariina: A study of seed dispersal and recruitment of plants in a

fragmented habitat. 1997:4 Jakobsson, Anna: Fecundity and abundance - a comparative study of grassland

species. 1997:5 Löfgren, Per: Population dynamics and the influence of disturbance in the

Carline Thistle, Carlina vulgaris. 1998:1 Mattsson, Birgitta: The stress concept, exemplified by low salinity and other

stress factors in aquatic systems. 1998:2 Forsslund, Annika & Koffman, Anna: Species diversity of lichens on

decaying wood - A comparison between old-growth and managed forest. 1998:3 Eriksson, Åsa: Recruitment processes, site history and abundance patterns of

plants in semi-natural grasslands. 1998:4 Fröborg, Heléne: Biotic interactions in the recruitment phase of forest field

layer plants. 1998:5 Löfgren, Anders: Spatial and temporal structure of genetic variation in plants. 1998:6 Holmén Bränn, Kristina: Limitations of recruitment in Trifolium repens. 1999:1 Mattsson, Birgitta: Salinity effects on different life cycle stages in Baltic and

North Sea Fucus vesiculosus L. 1999:2 Johannessen, Åse: Factors influencing vascular epiphyte composition in a lower

montane rain forest in Ecuador. An inventory with aspects of altitudinal distribution, moisture, dispersal and pollination.

1999:3 Fröborg, Heléne: Seedling recruitment in forest field layer plants: seed production, herbivory and local species dynamics.

1999:4 Franzén, Daniel: Processes determining plant species richness at different scales - examplified by grassland studies.

1999:5 Malm, Torleif: Factors regulating distribution patterns of fucoid seaweeds. A comparison between marine tidal and brackish atidal environments.

1999:6 Iversen, Therese: Flowering dynamics of the tropical tree Jacquinia nervosa. 1999:7 Isæus, Martin: Structuring factors for Fucus vesiculosus L. in Stockholm south

archipelago - a GIS application. 1999:8 Lannek, Joakim: Förändringar i vegetation och flora på öar i Norrtälje

skärgård. 2000:1 Jakobsson, Anna: Explaining differences in geographic range size, with focus

on dispersal and speciation. 2000:2 Jakobsson, Anna: Comparative studies of colonisation ability and abundance in

semi-natural grassland and deciduous forest. 2000:3 Franzén, Daniel: Aspects of pattern, process and function of species richness in

Swedish seminatural grasslands. 2000:4 Öster, Mathias: The effects of habitat fragmentation on reproduction and

population structure in Ranunculus bulbosus. 2001:1 Lindborg, Regina: Projecting extinction risks in plants in a conservation

37

context. 2001:2 Lindgren, Åsa: Herbivory effects at different levels of plant organisation; the

individual and the community. 2001:3 Lindborg, Regina: Forecasting the fate of plant species exposed to land use

change. 2001:4 Bertilsson, Maria: Effects of habitat fragmentation on fitness components. 2001:5 Ryberg, Britta: Sustainability aspects on Oleoresin extraction from

Dipterocarpus alatus. 2001:6 Dahlgren, Stefan: Undersökning av fem havsvikar i Bergkvara skärgård, östra

egentliga Östersjön. 2001:7 Moen, Jon; Angerbjörn, Anders; Dinnetz, Patrik & Eriksson Ove:

Biodiversitet i fjällen ovan trädgränsen: Bakgrund och kunskapsläge. 2001:8 Vanhoenacker, Didrik: To be short or long. Floral and inflorescence traits of

Bird`s eye primrose Primula farinose, and interactions with pollinators and a seed predator.

2001:9 Wikström, Sofia: Plant invasions: are they possible to predict? 2001:10 von Zeipel, Hugo: Metapopulations and plant fitness in a titrophic system –

seed predation and population structure in Actaea spicata L. vary with population size.

2001:11 Forsén, Britt: Survival of Hordelymus europaéus and Bromus benekenii in a deciduous forest under influence of forest management.

2001:12 Hedin, Elisabeth: Bedömningsgrunder för restaurering av lövängsrester i Norrtälje kommun.

2002:1 Dahlgren, Stefan & Kautsky, Lena: Distribution and recent changes in benthic macrovegetation in the Baltic Sea basins. – A literature review.

2002:2 Wikström, Sofia: Invasion history of Fucus evanescens C. Ag. in the Baltic Sea region and effects on the native biota.

2002:3 Janson, Emma: The effect of fragment size and isolation on the abundance of Viola tricolor in semi-natural grasslands.

2002:4 Bertilsson, Maria: Population persistance and individual fitness in Vicia pisiformis: the effects of habitat quality, population size and isolation.

2002:5 Hedman, Irja: Hävdhistorik och artrikedom av kärlväxter i ängs- och hagmarker på Singö, Fogdö och norra Väddö.

2002:6 Karlsson, Ann: Analys av florans förändring under de senaste hundra åren, ett successionsförlopp i Norrtälje kommuns skärgård.

2002:7 Isæus, Martin: Factors affecting the large and small scale distribution of fucoids in the Baltic Sea.

2003:1 Anagrius, Malin: Plant distribution patterns in an urban environment, Södermalm, Stockholm.

2003:2 Persson, Christin: Artantal och abundans av lavar på askstammar – jämförelse mellan betade och igenvuxna lövängsrester.

2003:3 Isæus, Martin: Wave impact on macroalgal communities. 2003:4 Jansson-Ask, Kristina: Betydelsen av pollen, resurser och ljustillgång för

reproduktiv framgång hos Storrams, Polygonatum multiflorum. 2003:5 Sundblad, Göran: Using GIS to simulate and examine effects of wave exposure

on submerged macrophyte vegetation.

38

2004:1 Strindell, Magnus: Abundansförändringar hos kärlväxter i ädellövskog – en jämförelse av skötselåtgärder.

2004:2 Dahlgren, Johan P: Are metapopulation dynamics important for aquatic plants? 2004:3 Wahlstrand, Anna: Predicting the occurrence of Zostera marina in bays in the

Stockholm archipelago,northern Baltic proper. 2004:4 Råberg, Sonja: Competition from filamentous algae on Fucus vesiculosus –

negative effects and the implications on biodiversity of associated flora and fauna.

2004:5 Smaaland, John: Effects of phosphorous load by water run-off on submersed plant communities in shallow bays in the Stockholm archipelago.

2004:6 Ramula Satu: Covariation among life history traits: implications for plant population dynamics.

2004:7 Ramula, Satu: Population viability analysis for plants: Optimizing work effort and the precision of estimates.

2004:8 Niklasson, Camilla: Effects of nutrient content and polybrominated phenols on the reproduction of Idotea baltica and Gammarus ssp.

2004:9 Lönnberg, Karin: Flowering phenology and distribution in fleshy fruited plants.

2004:10 Almlöf, Anette: Miljöfaktorers inverkan på bladmossor i Fagersjöskogen, Farsta, Stockholm.

2005:1 Hult, Anna: Factors affecting plant species composition on shores - A study made in the Stockholm archipelago, Sweden.

2005:2 Vanhoenacker, Didrik: The evolutionary pollination ecology of Primula farinosa.

2005:3 von Zeipel, Hugo: The plant-animal interactions of Actea spicata in relation to spatial context.

2005:4 Arvanitis, Leena T.: Butterfly seed predation. 2005:5 Öster, Mathias: Landscape effects on plant species diversity – a case study of

Antennaria dioica. 2005:6 Boalt, Elin: Ecosystem effects of large grazing herbivores: the role of nitrogen. 2005:7 Ohlson, Helena: The influence of landscape history, connectivity and area on

species diversity in semi-natural grasslands. 2005:8 Schmalholz, Martin: Patterns of variation in abundance and fecundity in the

endangered grassland annual Euphrasia rostkovia ssp. Fennica. 2005:9 Knutsson, Linda: Do ants select for larger seeds in Melampyrum nemorosum? 2006:1 Forslund, Helena: A comparison of resistance to herbivory between one exotic

and one native population of the brown alga Fucus evanescens. 2006:2 Nordqvist, Johanna: Effects of Ceratophyllum demersum L. on lake

phytoplankton composition. 2006:3 Lönnberg, Karin: Recruitment patterns, community assembly, and the

evolution of seed size. 2006:4 Mellbrand, Kajsa: Food webs across the waterline - Effects of marine subsidies

on coastal predators and ecosystems. 2006:5 Enskog, Maria: Effects of eutrophication and marine subsidies on terrestrial

invertebrates and plants. 2006:6 Dahlgren, Johan: Responses of forest herbs to the environment.

39

40

2006:7 Aggemyr, Elsa: The influence of landscape, field size and shape on plant species diversity in grazed former arable fields.

2006:8 Hedlund, Kristina: Flodkräftor (Astacus astacus) i Bornsjön, en omnivors påverkan på växter och snäckor.

2007:1 Eriksson, Ove: Naturbetesmarkernas växter- ekologi, artrikedom och bevarandebiologi.

2007:2 Schmalholz, Martin: The occurrence and ecological role of refugia at different spatial scales in a dynamic world.

2007:3 Vikström, Lina: Effects of local and regional variables on the flora in the former semi-natural grasslands on Wäsby Golf club’s course.

2007:4 Hansen, Joakim: The role of submersed angiosperms and charophytes for aquatic fauna communities.

2007:5 Johansson, Lena: Population dynamics of Gentianella campestris, effects of grassland management, soil conditions and the history of the landscape

2007:6 von Euler, Tove: Sex related colour polymorphism in Antennaria dioica. 2007:7 Mellbrand, Kajsa: Bechcombers, landlubbers and able seemen: Effects of

marine subsidies on the roles of arthropod predators in coastal food webs. 2007:8 Hansen, Joakim: Distribution patterns of macroinvertebrates in vegetated,

shallow, soft-bottom bays of the Baltic Sea. 2007:9 Axemar, Hanna: An experimental study of plant habitat choices by

macroinvertebrates in brackish soft-bottom bays. 2007:10 Johnson, Samuel: The response of bryophytes to wildfire- to what extent do

they survive in-situ? 2007:11 Kolb, Gundula: The effects of cormorants on population dynamics and food

web structure on their nesting islands. 2007:12 Honkakangas, Jessica: Spring succession on shallow rocky shores in northern

Baltic proper. 2008:1 Gunnarsson, Karl: Påverkas Fucus radicans utbredning av Idotea baltica? 2008:2 Fjäder, Mathilda: Anlagda våtmarker i odlingslandskap- Hur påverkas

kärlväxternas diversitet? 2008:3 Schmalholz, Martin: Succession in boreal bryophyte communities – the role of

microtopography and post-harvest bottlenecks. 2008:4 Jokinen, Kirsi: Recolonization patterns of boreal forest vegetation following a

severe flash flood. 2008:5 Sagerman, Josefin: Effects of macrophyte morphology on the invertebrate

fauna in the Baltic Sea. 2009:1 Andersson, Petter: Quantitative aspects of plant-insect interaction in

fragmented landscapes – the role of insect search behavior.

Abstract Seabirds have profound effects on plants and animals on their nesting islands by depositing

large amounts of nitrogen and phosphorus rich guano and providing their living and dead

bodies. Several previous studies have investigated vegetation responses and responses by

specific arthropod species and lizards to seabird colonies, but our study is the first to include

both plants and all major aboveground arthropod groups. To identify major pathways in the

island food webs, we used the different carbon isotope signals from terrestrial plants and

algae, and the strong nitrogen isotope signal from guano. Firstly, we found that food web

consequences on land also depend on processes in surrounding water bodies. Major predators

on the islands, such as spiders, utilise marine food items to a high extent, mainly chironomids

but to a lesser extent also terrestrial detritivores feeding on algal detritus on the shore. As a

consequence, density changes in marine invertebrates due to cormorants may affect predator

densities on land. Secondly, decreased vegetation cover and increased plant nutrient content

on active cormorant islands affected three of five investigated herbivore taxa. Lepidopteran

larvae and aphids increased and herbivore beetles decreased on active cormorant islands. The

effects on aphid densities cascaded up to an increased coccinelid density. In contrast to active

cormorant islands, abandoned islands had a higher plant biomass than non-bird islands. The

two arthropod groups that seemingly responded to this increased plant biomass were

lepidopterens and web-building spiders. Thirdly, the decreased vegetation cover on active

cormorant islands seemingly has direct negative consequences for some predators, such as

ground living lycosid spiders. This negative effect through vegetation cover might be one

reason why we did not find increased densities of predator on active cormorant islands despite

increased prey (chironomids and brachycerid flies) densities.

41

Introduction

Seabirds play an important role as consumers in coastal ecosystems and as vectors

connecting the marine and the terrestrial ecosystems (Furness and Cooper 1982; Duffy and

Siegfried 1987; Schneider et al. 1987; Polis et al. 2004; Ellis et al. 2006). They transport

nutrients and carbon from the marine to the terrestrial system through their carcasses, feathers,

reproductive by-products, food-scrapes and waste products, and as N- and P- rich guano

(Siegfried et al. 1978; Williams and Berruti 1978; Anderson and Polis 1999; Sanchez-Pinero

and Polis 2000; Wait et al. 2005; Hobara et al. 2005). It has been estimated that 104-105 tons

of P are transferred by seabirds from aquatic systems to land annually (Hutchinson 1950). Not

surprisingly, soils and plants nearby seabird colonies are typically highly enriched in N and P,

affecting both plant biomass and plant species composition (Gillham 1956; Smith 1978;

Anderson and Polis 1999; Garcia et al. 2002; Ellis et al. 2005, 2006; Wait et al. 2005). Areas

near seabird colonies are mostly species poorer than areas without seabird, whereas the

aboveground biomass is greater in seabird influent areas, expect in areas with extremely high

nest densities (Ellis et al. 2005, 2006; Wait et al. 2005; Elser et al. 2007).

Effects on primary producers cascade up the food web and affect consumers at several

trophic levels (Sanchez-Pinero and Polis 2000; Mulder and Keall 2001; Barrett et al. 2005). A

high nitrogen and phosphorus availability may affect arthropod densities positively through

changes in both plant quantity and quality (Siemann 1998; Siemann et al. 1998; Zvereva and

Rank 2003; Kagata et al. 2005). At the same time, high guano deposition may also negatively

affect arthropod density and diversity via changes in the structure of habitats and in the

density and composition of primary food sources. For instance, seabirds represent a high

quality food source for scavengers and parasites, increasing their densities (Siegfried et al.

1978; Duffy 1983; Sanchez-Pinero and Polis 2000). Specific predictions about seabird effects

on the food web are however complicated by additional marine-land interchanges. Run-off

from islands of mainly nitrogen may increase algal production around the islands, and

indirectly increase the production of aquatic insects, such as chironomids. In the Baltic, high

numbers of chironomids provide alternative food sources for island predators and detritivores

(Mellbrand et al. in prep). To develop predictions about cormorant effects on island food

webs therefore requires information about the structure of island food webs, the fate of the

avian nitrogen and the importance of marine versus terrestrial prey for different predatory

groups.

Stable isotope analysis has become a popular tool for ecologists to elucidate the structure

42

of food webs, to calculate the importance of marine food versus terrestrial food sources for

terrestrial consumers and to trace the fate of avian nitrogen (Lindeboom 1984; Anderson and

Polis 1998; Wainright et al. 1998; Paetzold et al. 2008). Heavier isotopes of carbon and

nitrogen are concentrated in water (Peterson and Fry 1987), and therefore, marine primary

producers and their consumers show higher δ13C values than terrestrial plants and their

consumers (Paetzold et al. 2005). Nitrogen in the guano of fish-eating seabirds is strongly

enriched in 15N because of their high trophic position and the fast mineralization of uric acid

to ammonium (NH4) and its resulting large isotopic fractionation (Lindeboom 1984;

Wainright et al. 1998; Barrett et al. 2005). This isotope enrichment also translates into

enriched δ15N signatures of soils, plants and their consumers in cormorant effected areas

(Barrett et al. 2005).

In this study, we investigated the effects on cormorants (Phalarocorax carbo) on the

food web of their nesting islands in the archipelago of Stockholm. We compared active

cormorant islands with different nest densities, recently abandoned nesting islands and islands

without nesting colonies. We chose cormorants because of 1) their increasing numbers in

Europe, in contrast to most other seabird species, 2) their high public interest and 3) the

scientific knowledge gap of their impact on nesting islands especially in temperate climates.

Firstly, we used stable isotope analysis to delimit the food web structures on island on the

different island types and trace the fate of marine N and C. Secondly; we examined biomass

and density responses on plants and arthropods along the gradient of cormorant nesting

densities. Specifically, we examined the following questions: 1) How do cormorants affect the

aboveground plant biomass and the nitrogen content of the plant? 2) What are the main prey

sources of different predator groups? Which predators feed mainly on terrestrial herbivores

and detritivores and which predators feed mainly on emerging insects with aquatic larvae? 3)

Do predators change diet in response to changes in prey availability on control versus

cormorant nesting islands? 4) Do cormorants affect the density of herbivorous, detritivorous

and predatory arthropods respectively?

43

Material and methods

Study site

The study was conducted on 19 islands in the northern part of the Stockholm archipelago,

Sweden (Fig. 1). The archipelago consists of about 24 000 islands with sizes varying between

less than one square-meter and several square-kilometers. The archipelago is subjected to

isostatic rebound, currently at a rate of 0.47 cm/year (Ericson and Wallentinus 1977),which

means that the islands are relatively young (Lofgren and Jerling 2002). The bedrock of study

islands consists of granite-gneiss, with a mostly very thin soil layer. The vegetation differs

from island to island; some islands are only covered with bare rocks, others with herbs and

grasses or even forests. The first cormorants (Phalacrocorax carbo) recolonized the

archipelago 1994 after hundreds years of absence and increased strongly in numbers until

2006, where after their population size seemed to have stabilized. During April to August,

cormorants are largely confined in colonies; about 20 colonies in the entire archipelago with a

total of 5 234 nests (Länsstyrelsen 2005, Staav 2007). For this study, we chose seven active

and three abandoned cormorant nesting islands in a subsection of the archipelago, and nine

structurally similar, but neighboring, islands without nesting cormorants and therefore

categorized as non-bird (control) islands. The islands differ in size (0.3-2.7 ha), distance from

the mainland (0.1 and 18 km) and vegetation, but we tried to choose appropriate control

islands in relation to the cormorant islands (Tab. 1). The nest density in the active cormorant

colonies ranged from 0.007 to 0.063 nest/m² and the time span since colonization was four to

ten years. We grouped the active cormorant island according to their nest density in two

categories: islands with a low nest density (<0.4 nests/m²) and islands with a high nest density

(> 0.04 nests/m²).

44

Tab 1: Summary of the 19 study island (*1-6 location of the island marked in the map in Fig.1.)

area

(m2)

number of active

cormorant nests

Density

(2007)

(nest/m2)

time span of

active

colonization

Stable

isotope

sampling

2005 2006 2007

cormorant islands

Marskärskobben*3 7164 81 186 177 0.025 2003-2008 Yes

St.Halmören*4 8091 222 0 0 0.000 2002-2005 Yes

St.Träskär*4 15729 80 50 0 0.000 1996-2005 Yes

Kattören*5 3264 0.000 1997-2000 No

N.Småholmen*1 8550 410 591 538 0.063 2000-2008 Yes

S.Småholmen*1 7012 176 194 188 0.027 1998-2008 No

N.Ryssmasterna*1 3224 65 171 127* 0.040 2003-2008 Yes

S.Ryssmasterna*1 3687 61 0.017 ?-2008 No

Bergskäret*2 22728 555 595 656 0.029 1998-2008 Yes

Delö*6 1702 37 42 13 0.007 2002-2008 Few

non-cormorant islands

Fårörarna*3 3286 Yes

Norröra*4 12475 No

Ägglösen*4 17357 Yes

V.Mellgrund*4 3889 Yes

Ljusstaken*5 5525 No

Hannasholmen *1 7743 Few

Nickösörarna*1 5209 Yes

Mjölingsören*2 27285 Yes

Ostkanten*6 2337

No

45

Stockholm

**1 *2

*3

*4*5

*6

Fig. 1: Map showing the location of the study island in the northern part of archipelago of Stockholm, Sweden. (*1 S. and N. Småholmen, S. and N. Ryssmasterna, Hannaholmen, Nickosören; *2 Bergskäret and Mjölingsören; *3 Marskärskobben and Fårören; *4 S. Träskär, S.Halmören, V. Mellgrund, Norröra, Ägglösen; *5 Kattören and Ljusstaken and *6 Delö and Ostkanten). For description of islands see tab. 1.

Sampling and processing

Vegetation and rock cover was estimated by walking the islands along 1-2 transect lines in

July 2007. Based on the percentage vegetation cover along the transects the percentage

vegetation cover of the whole island was estimated. To estimate plant biomass in the herb

layer, we collected, dried (50 oC, 72 h) and weighed all green plant material from 20 plots (25

cm x 25 cm), randomly positioned along the transects. Hence, the estimated plant

aboveground biomass describes the average biomass across the entire island. The nitrogen

content was measured in connection with the stable isotope analysis.

Arthropod densities were estimated in August 2007 by sampling ten points (within a 0.7

m² frame) on each island, using a converted leaf blower (Stihl® BG85 Leaf Blower/VAC).

All sampling points were chosen within intact vegetation, and raw density estimates therefore

represent density per unit intact vegetation. The samples were stored in the freezer until they

were sorted, identified to species, family or order level (depending on taxa) and weighed. For

every island, we calculated the mean number of individuals and mean weight per 0.7 m²

vegetated area. Based on the estimated vegetation cover, we also estimated the density of

arthropods across the entire island area by multiplying the mean arthropod densities per unit

vegetated area with the island vegetation cover. We did not do this correction for dipterans

because of their independency of ground vegetation.

Sample specimens from the D-Vac sampling were complemented with hand collection,

46

sweep netting and pit-fall traps in July and August 2006-2008, to collect samples for stable

isotope analyses. Stable isotope sampling was mainly done on 11 study islands, with some

additional samples from remaining study islands, in at least three plots per islands. Up to five

samples were collected for the following groups, that were all common on islands: terrestrial

plants (Tanacetum vulgaris, Filipendula ulmaria, Sorbus aucuparia, Alnus glutinosa,

Juniperus communis, Poaceae, mosses) and terrestrial arthropods from several trophic levels

(Insects with aquatic larvae, chiromomids and trichopterans; Detritivores, brachycerid flies,

isopods; Omnivores: ants; Herbivores: homopterans [aphids and cicadas], heteropterans

[Miridae], lepidopteran larvae; Predators: beetles [Carabidae, Staphylinidae and

Coccinellidae], Nabidae, Chilopoda and four spider families [Lycosidae, Araneidae,

Linyphiidae and Tetragnathidae (Tetragnatha and Pachygnatha)] ). We grouped Araneidae,

Linyphiidae and Tetragnatha under web-building spiders. In order to calculate the importance

of marine algae as a food source for terrestrial detritivores, flies and isopods, we also

collected six fronds of the dominant brown macro algae (Fucus vesiculosus) and its epiphytic

algae in one to five meter distance to the islands.

Animals were freeze-dried, vascular plants and algae oven-tried (50°C, up to two

weeks’) prior to analysis. Plant and animal specimens were analyses individually, but pooled

samples were occasionally used for arthropod taxa with individual dry weights less than 0.7

mg. When possible, only legs and wings were used to avoid including gut contents. The

samples were sent to UC Davis Stable Isotope facility, California, USA and the stable isotope

ratios for carbon and nitrogen were measured by using an Isotope Ratio Mass Spectrometer

type Europa integra. Isotope ratios were calculated as deviation from the international

limestone standard Vienna PeeDee Belemnite (VPDB) (δ13C) and atmospheric N (δ15N) in

delta (δ) units in part per thousand (‰):

δX = [(Rsample/Rstandard)-1] * 1000

where X is the heavier isotope of the element (13C or 15N) and R is the corresponding isotopic

ratio (13C/12C or 15N/14N).

Stable isotope analysis

Consumers typically reflect the stable isotope composition of their food source with some

predictable changes (fractionation). In general, carbon isotope ratios change only little

between trophic levels, whereas the nitrogen isotope ratios show more distinct increases

(McCutchan et al. 2003; Vanderklift and Ponsard 2003). Carbon isotope ratios are clearly

separated between marine and terrestrial plants, whereas nitrogen isotope ratios show a much

47

larger variability. Carbon isotope ratios are therefore an often more predictable source for

identifying the relative importance of marine and terrestrial carbon for consumers (Barrett et

al. 2005). Fish-eating cormorants have, however, according to their relatively high trophic

position strongly elevated δ15N values (Barrett et al. 2005). This difference is further

enhanced through the fast mineralization of uric acid to ammonium (NH4), a chemical

reaction that selectively removes 14N from guano (Lindeboom 1984; Wainright et al.. 1998).

Stable isotope values of nitrogen can therefore be used to trace the fate of avian nitrogen on

and around islands.

Based on the δ13C and δ15N in possible food sources, it is possible to estimate the

relative proportion of marine and terrestrial carbon in higher trophic level with the help of

mixing models (Phillips and Gregg 2001). The use of diet mixing models can be problematic,

if the trophic fractionations of δ13C and δ15N for the study consumers are unknown.

Especially the fractionation of N varies strongly among species, among tissues within a single

species, among diets and among ration size (McCutchan et al. 2003; Vanderklift and Ponsard

2003; Barnes and Jennings 2007). Using wrong fractionation factors in diet mixing models

result in errors in estimated diet proportion (Wolf et al. 2009). In our study, the trophic

fractionations of the investigated taxa were unknown, but we assumed a high variability in the

fractionation of δ 15N, both between the taxa and between the island categories. The

fractionation of δ13C is known to vary as well but to a lower degree. We tested the use of dual

isotopes (δ13C, δ15N) three source mixing models with chironomids, flies and terrestrial

herbivores as baseline to estimate the relative diets of predators. The impossible results

(highly negative and positive values for the different prey species) caused us to refrain from

using δ15N within mixing models.

As an alternative approach, we first compared the stable isotope signatures of plants and

arthropods from three island categories (control island, abandoned cormorant island and

active cormorant island) with linear mixed effect modeling. Carbon and nitrogen isotope

signatures were analyzed separately, with island category as fixed factor and islands as

random factor. We then used single isotope (δ13C), two-source diet mixing models to estimate

the relative proportion of marine and terrestrial carbon in the bodies of detritivores and

predators. For this analysis, we used terrestrial plants and epiphytic algae as baseline and

assumed a trophic fractionation of 0.4‰ (McCutchan et al. 2003). We used the information

from these two approaches to construct a preliminary food web for islands with active

cormorant colonies.

48

Density response analysis

To test the cormorant effect on the vegetation, we first correlated vegetation cover with the

active cormorant nest density and then compared the aboveground biomass of the three island

categories in an ANOVA. To investigate the effect of cormorant colonies (active and

abandoned) on the structure of island food webs, we first performed MANOVAs with Pillai-

Bartlett statistic for densities of the three major arthropod groups; herbivores, detritivores and

predators, separately, using island category (categorical), island size (loge-transformed),

distance from the mainland (loge-transformed) and their interactions as explanatory variables.

Non-significant variables (p>0.1) were excluded from the final model. Significant variables

were then used in ANCOVAs to test the response of the individual groups from the three

trophic levels. Families which were not included in MANOVA (chironomids, ants, fungivores

and saprophagous beetles) were also analyzed with an ANCOVA. They were tested against

the maximal model, including the same variables as in the MANOVA. To detect differences

in arthropod biomass at major trophic level between island categories, we used ANCOVAs,

with island category (categorical), island size (loge-transformed), distance from the mainland

(loge-transformed) and their interaction as explanatory variables. As in the previous analysis,

variables not improving the models were excluded. All arthropod densities and weights tested

in the main analyses were estimates per unit vegetated area. In an additional analysis, we

tested arthropod densities estimated for the whole island area. For all statistical analyses, we

used the free software R. 2.4.0 (R Development Core Team 2007).

.

Results

Vegetation

The vegetation cover decreased significantly (R²=57.0%, t=-4.99, p<0.001, Fig. 2) with the

active cormorant nesting density, but the cover of abandoned islands was equal to that on

control islands (Fig. 2). In contrast, the aboveground biomass was 2.4 times higher on

abandoned cormorant islands than on control islands (F=3.4, p=0.060, R²=20.1). The plants

on islands with active cormorant nesting colonies was 1.6 (herbs) – 2.6 (Sorbus aucuparia)

times higher than the nitrogen content of plants on non-bird islands (t=3.0–5.8, p<0.02 for all

tests). The nitrogen content of plants on islands with abandoned cormorant colonies was about

equal to plants on non-bird islands.

49

0

0.2

0.4

0.6

0.8

1

1.2

0 0.01 0.02 0.03 0.04 0.05 0.06 0.07

cormorant nest density (nest/m²)

% v

eget

atio

n co

ver

Fig.2: Relation between vegetation cover and cormorant nest density on 19 islands with active and abandoned cormorant islands and on control islands without cormorant colonies in the archipelago of Stockholm, Sweden.

Stable isotope analysis

The stable isotope composition of nitrogen was distinctly higher for all trophic levels on

active cormorant islands than on control islands (Tab. 2, Fig. 3). Detritivores showed the

highest increase (∆δ15N=15.1±1.3‰), followed by plants (∆δ15N=11.9±1.3‰) and herbivores

(∆δ15N=11.5±1.5‰). Predators had the lowest increase (∆δ15N=8.5±1.0‰), the lowest

increase of all terrestrial arthropods. However, the increase for chironomids from non-bird to

active cormorant island was even lower (δ15N=5.5±3.8‰). There was also a large variation

within groups. Different predatory groups showed a particularly big variation, ranging from

∆δ15N=5.1±1.6‰ in web-building spiders to ∆δ15N=16.2±3.1‰ in staphylinid beetles (Fig.

4). In general, predatory insects showed a higher ∆δ15N than spiders. Flies showed a higher

δ15N increase (∆δ15N=19.6±3.8‰) than other detritivores and the highest increase of all taxa.

When comparing isotopic enrichment among cormorant islands, it was apparent that

δ15N differed for some but not for all taxa on islands with low and high cormorant nest

density (Fig. 4, Appendix 1). Plants, herbivores, collembolans, coccinelids and carabids had

about equal δ15N on islands with low and high nest densities, whereas δ15N was higher for

algae, chironomids, isopods, flies, ants, staphylinids, nabids and spiders on islands with a high

nest density. Similarly, the isotopic enrichment varied between active and abandoned nesting

islands. Plants, herbivores, collembolans, coccinelids and carabids again responded similarly

and showed higher δ15N values on abandoned than on active cormorant islands, whereas the

δ15N signatures of all spiders, predatory bugs, chironomids and algae were about equal on

abandoned islands as on control islands. The δ15N values of ants, staphylinids, flies and

50

chilopods on abandoned islands were intermediate to those on control and active cormorant

islands. Finally, isopods had an about equal δ15N signature on abandoned islands as on active

cormorant islands.

For a few taxa, the δ13C values differed between island categories. Terrestrial plants,

flies, ants, coccinelids had between 1.2±0.4‰ (plants) and 2.6±0.9 ‰ (Coccinelidae) higher

δ13C values on active cormorant islands than on control islands. In contrast, butterfly larvae,

araneids and lycosids had between 1.6±0.7 and 3.2±1.2 ‰ lower δ13C values on islands with a

high nest density than on control islands. Araneids, nabids and ants had furthermore increased

δ13C values on islands with an abandoned cormorant colony.

Tab. 2: Stable isotope signature of carbon (δ13C) and nitrogen (δ15N) for plant and arthropod communities [mean±SE] on island with active and abandoned cormorant colonies and islands without seabird colonies in the archipelago of Stockholm, Sweden. Test statistics from linear mixed effects models. Sample sizes are provided in parentheses.

trophic group non-bird island abandoned cormorant island active cormorant island

t p t p

δN (‰)

Fucus vesiculosus 5.9±1.5 (66) 4.2±2.9 (24) -0.60 0.567 12.3±2.3 (48) 2.78 0.024

epiphytic algae 3.8±1.8 (29) 2.1±3.3 (12) -0.52 0.612 10.7±2.7 (24) 2.60 0.032

terr.plants 1.6±0.9 (85) 15.9±1.8 (29) 8.17 0.000 13.3±1.3 (61) 9.03 0.000

herbivores 4.0±1.0 (33) 20.9±1.6 (28) 10.57 0.000 11.5±1.6 (30) 7.70 0.000

detritivores 4.3±0.9 (39) 11.1±1.4 (21) 7.55 0 19.5±1.3 (40) 12.16 0

Chironomidae 6.2±1.2 (14) 4.6±1.6 (11) -0.90 0.374 11.7±1.8 (12) 3.11 0.014

predators 7.0±0.7 (161) 10.4±1.2 (71) 2.74 0.006 14.8±1.1 (119) 8.10 0.000

saprophagous beetles 21.8±0.6 (14)

δC(‰)

Fucus vesiculosus -12.0±0.4 (66) -11.2±0.8 (24) -12.2±0.6 (48)

epiphytic algae -19.1±0.7 (29) -19.1±1.2 (12) -19.1±1.0 (24)

terr.plants -29.2±0.3 (85) -29.1±0.5 (29) -27.9±0.4 (61) 3.14 0.007

herbivores -27.4±0.3 (33) -27.4±0.4 (28) -27.1±0.4 (30)

detritivores -23.4±0.5 (39) -23.5±0.8 (21) -22.1±0.7 (40) 1.91 0.078

Chironomidae -19.8±0.8 (14) -19.8±1.1 (11) -21.0±1.2 (12)

predators -22.6±0.5 (161) -20.6±0.9 (71) 2.27 0.024 22.7±0.8 (119)

saprophagous beetles -23.3±0.4 (14)

51

δ13C (‰)

δ15N

(‰

)

non-bird island

abandoned cormorant island

active cormorant island

0

5

10

15

20

25

-30 -25 -20 -15

pl

H D

O P

ep

Ch

ep

ep

Ch

ChP

O

O

pl

pl

H

H S

D

D

P

Fig. 3. The relationship between δ15N and δ13C values for plant and arthropod communities on island with active and abandoned cormorant colonies and islands without seabird colonies in the archipelago of Stockholm, Sweden. (ep=epiphytic algae, pl=terrestrial plants, M=emerging insects with aquatic larvae (Chironomidea), , D=detritivores, H=herbivores, P=predators, S=saprophagous beetles).

52

-20

0

5

10

15

20

25

30

-30 -25

δ15 N

( ‰

)

-15

δ13C (‰)

Co

Co

Co

Ca

Ca

A

Ca

A

A

0

5

10

15

20

25

30

-30 -25 -20 -15

St

S

C

N

St

C

St

NSS

CN

N

δ13C (‰)δ13C (‰)

0

5

10

15

20

25

30

-30 -25 -20 -15

δ15

N(

‰)

0

5

10

15

20

25

30

-30 -25 -20 -15

δ13C (‰)

L

L

L

LW

W

W

WP P

Pδ15 N

( ‰

)δ

15N

( ‰

)c) predatory insects d) spiders

b) predatory insects

a) herbivores+detritivores

non-bird islandabandoned cormorant islandactive cormorant island with a low nest densityactive cormorant island with a high nest density

herbivoresCollembolabrachycerid fliesChironomidaescavengers

Fig. 4. The relationship between δ15N and δ13C for arthropods on island with abandoned and active cormorant colonies with a low (<0.4 nests/m²) and a high (>0.4 nests/m²) nest density and islands without a seabird colony in the archipelago of Stockholm, Sweden. (b: C=Chilopoda, N=Nabidae, S=Saldidae, St=Staphylinidae; c: A=ant (Formicidae) ,Ca=Carabidae, Co=Coccinelidae; d: W=web-building spiders, L=Lycosidae, P=Pachygnatha)

53

Mixing models

The two-source diet mixing models indicate that all spiders, staphylinids and saldid bugs had

a very high content of marine originating carbon in their bodies (63-90%). Flies, isopods and

nabids had a somewhat lower content of marine originating carbon in their bodies (55-58%,

Fig. 5). Chilopods had an about equal amount of marine and terrestrial carbon whereas

collembolans, carabids and ants mainly had terrestrial carbon in their bodies (59-65%).

Coccinelids fed to about 94% on terrestrial carbon. Several predator taxa seemed to change

their diet among island types. All spiders, chilopods and ants had the highest, collembols

lowest percentage of marine carbon in their bodies on abandoned cormorant islands.

Staphylinids, saldid bugs and flies had the highest proportion of marine carbon on islands

with an active cormorant colony.

0

0.2

0.4

0.6

0.8

1

1.2

Lin

yph

iida

e

Ara

ne

ida

e

Te

tra

gn

ath

a

Lyc

osi

da

e

Pa

chyg

na

tha

Ca

rab

ida

e

Sta

ph

ylin

ida

e

Na

bid

ae

Sa

ldid

ae

Ch

ilop

od

a

Co

ccin

elid

ae

an

ts

Flie

s

Iso

po

da

Co

llem

bo

la

% m

arin

e C

sou

rce

control island

abandoned cormorant island

active cormorant island

Fig.5. Proportion marine and terrestrial carbon in the diet of the main arthropod predator and detritivores groups based on two-source diet mixing models with marine epiphytic algae and terrestrial plants as baseline on island with active or abandoned cormorant colonies and on islands without seabird colonies in the archipelago of Stockholm, Sweden (means±SE).

Arthropod densities

All following results refer to arthropod densities and weights per unit vegetated area if not

explicit defined differently.

The community compositions of predators (F=3.0, p=0.017), herbivores (F= 4.4, p=0.003)

and detritivores (F=5.2, p=0.003) were all affected by cormorant colonies. The composition of

predators (F=13.0, p=0.001) and detritivores (F=4.4, p=0.03) were furthermore correlated

with the distance from the mainland, whereas the herbivore composition (F=4.4, p=0.019)

was correlated with island size.

54

Among herbivores, aphids showed the highest densities on active cormorant islands and

about the same densities on islands without active nesting cormorants (control islands and

abandoned cormorant islands). The highest density of butterfly larvae was also found on

active cormorant islands whereas their densities on control islands were significant lower than

on abandoned cormorant islands. The lowest density of herbivores beetles was found on

active cormorant islands and the highest on abandoned cormorant islands. Among

detritivores, flies were the only group to be significantly affected by the cormorant nest

density. Flies had the highest density on active cormorant islands, whereas the densities on

abandoned cormorant islands and on control islands did not differ from each other.

Saprophagous beetles had the highest density on active cormorant islands and about equal

densities on the two island categories without active nesting cormorants. Fungivore beetles

had higher densities on abandoned and active cormorant islands than on control islands if

excluding one control island from the analysis. The density of chironomids were highest on

active cormorant islands and about equal on the two other island categories. This difference in

density were only marginal significant, but an additional analysis showed, that chironomids

only had a higher density on islands with a high active nest density (Appendix 2). Isopod

densities did not differ between the three island categories. The density of fungivous beetles,

wolf-spiders, web-building spiders, other-spiders and carabids were positively correlated with

distance from mainland, while parasitic hymenoptera and fly densities showed a weak

negative correlation with distance from mainland. Saprophagous beetle density and

lepidoptera larvae were negatively correlated with island size. Among predator groups, wolf

spiders showed the lowest density on active cormorant islands and about equal densities on

control islands and abandoned nesting islands. The highest density of aphidophaga showed a

similar density distribution as aphid and was most dense on active cormorant islands. Their

densities on control islands and abandoned cormorant islands were also about equal. Parasitic

hymenoptera had the lowest density on control islands and the highest density on active

cormorant islands. Web-building spiders had the highest density on abandoned cormorant

islands and the lowest on control islands (Fig. 6, Tab.3, 4).

All investigated taxa showed qualitatively similar density responses when we corrected

for vegetation cover on the island (Appendix 3). This correction mainly affected densities on

active cormorant islands due to their lower vegetation cover. The negative density effects of

lycosids and herbivores beetles were even stronger for the cover corrected densities than for

density per unit vegetated area, whereas the positive density for aphids and lepidoptera larvae

were weaker but still significant. The only statistically significant changes occurred for

55

parasitiods, where the density response to cormorants was no longer significant when tested

on the cover-corrected densities.

Tab. 3: Mean arthropod density per 0.7m2 vegetated island on nine non-seabird islands (=control islands), on three islands with an abandoned cormorant colony and on seven island with an active cormorant colony in the archipelago of Stockholm, Sweden.

taxa log(area)

log(distance

from the

mainland)

island category model

Aphidoidae F=4.7 p=0.024 F=4.7 p=0.024 R2 =37.2

Lepidoptera larvae F=4.1 p=0.061 F=19.7 =0.000 F=14.5 p=0.000 R2 =74.4

herbivores beetles F=5.7 p=0.014 R2 =41.4

brachycerid flies F=9.42 p=0.008 F=14.1 p=0.000 F=12.5 p=0.000 R2 =71.5

saprophagous beetles F=8.2 p=0.012 F=9.6 p=0.002 F=9.1 p=0.001 R2=64.6

fungivores beetles F=6.9 p=0.007 R2=48.0

Chironomidae F=2.8 p=0.091 R2=25.9

web-building spiders F=4.2 p=0.059 F=4.6 p=0.028 F=4.4 p=0.020 R2=47.0

Lycosidae F=15.2 p=0.001 F=7.1 p=0.007 F=6.9 p=0.007 R2=48.0

other-spiders F=4.0 p=0.062 R2=19.0

Carabidae F=19.9 p=0.000 R2=53.9

Aphidophaga F=6.9 p=0.007 R2=46.4

parasitic hymenoptera F=4.26 p=0.057 F=3.7 p=0.051 F=3.9 p=0.034 R2=43.6

Tab. 4: Mean arthropods weight (mg) per 0.7m2 vegetated island between on non-seabird islands (=control islands), islands with abandoned and island with active cormorant colonies in the archipelago of Stockholm, Sweden. Different letters represent significant differences.

Mean density per 0.7 m² Control island Abandoned

cormorant island

Active

cormorant island

Wolf spiders A A B

Net-spiders A B AB

Aphidophaga A A B

Parasitic hymenoptera A AB B

aphids A A B

Butterfly larvae A B B

Herbivore beetles A A B

Brachycerid flies A A B

Fungivore beetles* A B C

Saprophagous beetles A A A

*without V.Mellgrund

56

0.5

1.0

2.0

Lycosidae

20.00.1 0.2 0.5 1.0 2.0 5.0 10.0 20.0

Distance to mainland (km) (scale is logged)

Density (ind/0.7m²) (scale is logged)

12

105

Web-building spiders

20.00.1 0.2 0.5 1.0 2.0 5.0 10.0 20.0

Distance to mainland (km) (scale is logged)

20.00.1 0.2 0.5 1.0 2.0 5.0 10.0 20.0

Distance to mainland (km) (scale is logged)

0.8

1.0

1.2

1 .4

1.6

1.8

. 60

Parasitic hymenoptera1

25

1020

20.00.1 0.2 0.5 1.0 2.0 5.0 10.0 20.0

Distance to mainland (km) (scale is logged)

Density (ind/0.7m²) (scale is logged)

Brachycerid flies

0.5

1.0

2.0

5.0

2000 5000 10000 20000

Island area (m²) (scale is logged)

Lepidoptera larvaeSaprophagous beetles0.

51.

01.

52 .

02

.53.

5

2000 5000 10000 20000

Island area (m²) (scale is logged)

10. 0

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

0.5

01

.01

.02.

02.

05

.05

.010

. 0

Aphidophaga

12

51

01

25

10

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

Density (ind/0.7m²) (scale is logged)

Herbivore beetles Aphids

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

0.5

01

.01

.02

.02

.05

.05

.010

. 010

. 00

.00

.05

05

00

20

0

Fungivore beetles

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

non-bird islandabandoned cormorant islandactive cormorant island

0.5

1.0

2.0

5.0

10.

020

.05

0.0

Controlisland

Abandonedcormorant

island

Activecormorant

island

Controlisland

Abandonedcormorant

island

Activecormorant

island

Density (ind/0.7m²) (scale is logged)

0.5

1.0

1.5

3.0

2.5

2.0

0.5

1.5

2.0

Chironomidae

me

an d

ensi

ty p

er

0.7

m2

ve

geta

ted

are

a (s

cale

is lo

gged

) m

ean

dens

ity p

er 0

.7m

2 ve

geta

ted

are

a

(sca

le is

logg

ed)

me

an d

ensi

ty p

er 0

.7m

2 ve

ge

tate

d a

rea

(sca

le is

logg

ed)

mea

n de

nsity

per

0.7

m2

ve

geta

ted

are

a

(sca

le is

log

ged

)

Fig. 6: Mean arthropod density per 0.7m2 vegetated island on non-seabird islands (=control islands), on islands with abandoned colonies and on island with active cormorant colonies in the archipelago of Stockholm, Sweden.

57

The total arthropod mass per 0.7 m2 vegetated area on islands differed somewhat from the

corresponding density responses. Only among herbivores and predators, but not among

detritivores, did mass vary with the cormorant nesting activity. The herbivore mass per unit

area was 3.5 times higher on active cormorant islands and a 1.7 times higher on abandoned

cormorant islands than on control islands. Islands which were far away from the mainland and

small had significant lowest predator mass. The affect of cormorants on the mass at the level

of families and functional groups was quite similar to the density response. Lepidopteran

larvae had the highest mass on active cormorant islands and the lowest on control islands.

Aphids had the highest mass on active cormorant islands and the lowest on abandoned

cormorant islands. The mass of herbivores beetles was lowest on active cormorant islands and

highest on abandoned cormorant islands. Flies showed the highest mass on active cormorant

islands and about equal mass on abandoned cormorant islands and on control islands.

Saprophagous beetles showed the same pattern with the highest mass on active cormorant

islands and equally low mass on the two other island categories. The mean weight of

chironomids, showed the same response as the mean density of chironomids. Their weight

were highest on active cormorant islands and about equal on the two other island categories.

This difference in density were only marginal significant, but an additional analysis showed,

that chironomids only had a higher density on islands with a high active nest density

(Appendix 2). Isopods and ants did not show any response. Wolf spiders had lowest mass on

active cormorant islands and an about equal mass on abandoned cormorant islands as on

control islands. Aphidophagous predators showed an exact opposite response with the highest

mass on active cormorant islands and an equal low mass on the two other island categories.

Web-spiders had a lower mass on active cormorant islands than on abandoned cormorant

islands and control islands. Finally, parasitic hymenoptera showed the lowest mass on control

islands and the highest mass on active cormorant islands.

The interaction between distance to the mainland and island size affected the mass of most

taxa. The smaller and farther away from the mainland, the lower was the mass of wolf spiders,

aphidophagous and herbivorous beetles and the higher the mass of aphids. The mass of

cicadas, fungivorous and carabid beetles was positively correlated with the distance from the

mainland. The mass of saprophagous beetles was negatively correlated with island size

(Appendix 4).

58

Discussion

Seabirds certainly have profound effects on plant and animals on their nesting islands by

depositing large amounts of nitrogen and phosphorus rich guano and providing their living

and dead bodies (Gillham 1956; Duffy 1983; Anderson and Polis 1999; Polis and Hurd 1995;

Sanchez-Pinero and Polis 2000; Polis et al. 2004; Barrett et al. 2005; Ellis 2005; Wait et al.

2005; Ellis et al. 2006). Most studies on plant communities from seabird affected areas

describe an increased productivity or biomass, except where nutrient loads got toxic due to

very high seabird densities or drought (Smith 1976; Anderson and Polis 1999; Sanchez-Pinero

and Polis 2000; Ellis 2005; Wait et al. 2005). Several previous studies have investigated

responses by specific arthropod species and lizards to seabird colonies (Polis and Hurd 1995,

Sanchez-Pinero and Polis 2000, Barrett et al. 2005) but our study is the first to include both

plants and all major aboveground arthropod groups. First, we were able to use the carbon

isotope signal from terrestrial plants and algae, and the nitrogen isotope signal from guano to

identify major pathways in the island food webs (Fig.7). Most interestingly, we show that in

order to understand food web consequences on land it is necessary to include also surrounding

water bodies. Major predators on the islands, such as spiders, utilise marine food items to a

high extent, mainly chironomids but to a lesser extent also terrestrial detritivores (flies)

feeding on algal detritus on the shore. Furthermore, some taxa seemed to change diet between

islands with and without a cormorant colony. Five taxonomic groups (Chilopoda, Nabidae,

Linyphiidae, Araneidae and Pachygnatha) had a higher relative consumption of marine prey

on islands with abandoned cormorant colonies, and two other taxonomic groups (Saldidae and

Staphylinidae) had a higher relative consumption of marine prey on islands with active

colonies. Second, our data also suggest that the decreased vegetation cover on islands with

active cormorant colonies has direct negative consequences for some predators, such as

ground living lycosid spiders.

Effects on the plant community showed striking contrasts between active and abandoned

colony islands. Our study show that plant cover decreased strongly (up to 80%) on islands

with nesting cormorants, but quickly recovered after abandonment. In fact, there was a strong

increase in plant biomass (2.4 times) on islands with abandoned colonies compared with

control islands. Moreover, the nitrogen content was 1.6-2.7 times higher in plants from active

cormorant islands than in plants from control islands or from abandoned colonies, as was also

observed in other studies (Anderson and Polis 1999; Ellis 2005). Such changes in the quantity

and quality of plant biomass are expected to affect consumers at higher trophic levels (Hunter

59

and Price 1992; Siemann 1998; Siemann et al. 1998; Pace et al. 1999; Haddad et al. 2000;

Zvereva and Rank 2003; Fonseca et al. 2005; Kagata et al. 2005), and this was to some extent

also observed in our study. Aphids and butterfly larvae seem mainly to profit from the

increased nitrogen content, as they showed the highest densities and the highest weights on

active cormorant islands. In contrast, herbivorous beetles seemed to suffer from the lower

vegetation cover on these islands, and this group rather increased in density on abandoned

islands. This effect was even stronger when densities were averaged across the islands, by

correcting the data with percentage vegetation cover. The positive effects on aphids and

butterfly larvae was however still apparent after this correction. On abandoned islands

lepidopteren larvae seemed to profit from increased plant biomass, with a higher density on

this island category than on control islands.

We expected not only herbivores but also detritivores – as reported by Sanchez-Pinero

and Polis (2000) – to respond to cormorant colonies. Detritivores can be affected by seabirds

in two separate ways, either directly through the consumption of seabird carcasses and by-

products or indirectly through the observed changes in the vegetation. In our study, only

brachycerid flies responded to cormorants, and they had an about five times higher density on

active cormorant islands than on islands without current colonies. The isotope data further

suggest that this increased density was mainly caused by a direct effect of cormorants and not

via the vegetation. Diptera is an extremely species rich family, including both bird parasites

and scavengers, so it is very likely that islands with nesting cormorants included species not

present on other islands. Another detritivorous taxa, isopods, also had highly enriched δ15N

signatures on active colonies, but isopods did not show any density response to cormorants.

The lack of density response of detritivores, other than flies, might be explained by their use

of other abundant detritivorous material, such as shore-drifted algae and terrestrial plants.

Shore-line predators also use aquatic prey sources beside terrestrial food sources

(Murakami and Nakano 2002; Sanzone et al. 2003). To study and explain the effect of nesting

cormorants on predators, we therefore first had to understand predator-prey relationships and

how prey availability was affected by cormorant colonies. The diet mixing models, and the

related changes in δ13C and δ15N in response to cormorants, suggest that all investigated web-

building spiders mainly prey on chironomids and possibly also on trichopterans, although the

latter are fairly rare on the islands. The density of chironomids was only affected by nesting

cormorants on active islands with a high nest density, where the chironomids showed an

increased density. Web-building spiders, however, did not show increased density on active

cormorant islands. This lack of positive density response was even more unexpected,

60

considering the high brachycerid fly density on these islands. The highest density of web-

spiders was instead found on abandoned cormorant islands where they fed, according to the

diet mixing model and their δ15N signature, mainly on chironomids. This behaviour can

neither be explained by the density of chironomids nor by their nitrogen content; which did

not differ among islands. However, web-building spiders on abandoned cormorant islands

might profit from increased lepidopteren density and increased habitat quality, through

increased plant biomass. The ground-living lycosid spiders differ in their ecology and

hunting method from web-building spiders. These differences are reflected in their response

to nesting cormorants. Lycosids seemingly prey, according to the diet mixing models and to

the higher δ15N signature on abandoned and active cormorant islands, to a lower degree on

chironomids. Their δ15N signature on islands with a high nest density is similar to the δ15N

signature of the sarcophagus beetle Omosita colon. This similarity indicates that lycosids

mainly fed on prey that in turn feed directly on cormorants, like scavengers or parasites,

possibly flies. Despite this diet and the high prey abundance on active cormorant islands,

lycosid spiders decreased in density on these islands. The most likely hypothesis is that

lycosids responded strongly to the decreased habitat quality within colonies, through the

reduction in vegetation cover.

Only one group of predatory insects, aphidopagous species, responded significantly to

cormorant colonies. Similar to aphids, their main prey, aphidophagous species showed the

highest density on active cormorant islands. Even though other predatory insect families did

not show numerical responses to cormorant colonies, some families seemingly changed their

diet under the effect of cormorant colonies. The diet mixing models indicate that nabid bugs,

like web-building spiders, increased their feeding of marine prey (likely chironomids) on

abandoned cormorant islands. Saldid bugs similarly had only marine carbon in their diet on

active cormorant islands. The δ15N value of saldid bugs was however similar to that of

lycosids, and could again indicate feeding on prey that feed directly on cormorant remnants.

Also staphylinids and chilopods seemed, according to their δ15N, to feed on such prey. The

lack of positive density response by the main predators in response to increased prey densities

on active cormorant islands might be, beside the direct negative habitat effects, a lack of food

limitation due to constantly high abundances of chironomids and detritivores. Carabid beetles

were beside coccinelids the predatory family which fed to the highest degree on terrestrial

prey, which is reflected in their isotopic signature intermediate between herbivores and

collembolans. The dominant carabid on islands is Dyschirius globosus, known to feed on

collembolans and other small ground-dwelling prey.

61

We can summarize our result with the statement that we found fewer effects of nesting

cormorant colonies on the arthropod food web than what the previous literature allowed us to

believe. Several studies have shown that nesting seabirds, due to their guano deposition,

change the nutrient composition in the soil and mainly increase nitrogen and phosphorus

content (Smith 1978; Wait et al. 2005; Ellis 2005). Nitrogen and phosphorus are important

limiting factors in the productivity of many ecosystems (Mattson 1980; Vitousek and

Howarth 1991; Pennington et al. 2006; Elser et al. 2007), and the strong nutrient input on

cormorant nesting islands should cascade up the food web (Hunter and Price 1992; Pace et al.

1999). Despite this expectation, we found only one clear case of bottom-up control via guano

– plant – aphids – aphidophages, one possible guano-plant-butterflies-web-building spiders

and no case of bottom-up control via seabird bodies – parasites/scavengers – spiders despite

the increased dipteren densities within active cormorant colonies.

Even though cormorant islands could in some ways be seen as natural long term

fertilisation experiments, our study system differ in some important aspects from such

experimental sites. Firstly, the nutrient load on cormorant islands is typically much higher

than in most fertilization experiments and less evenly distributed. This high nitrogen load

leads to toxic loads within some patches on the islands and this toxicity likely constrained the

vegetation growth and seed germination and killed invertebrates (see also Mulder & Keall

2001; Ellis et al. 2006). Studies which found positive effects by seabirds on the biomass of

the aboveground vegetation within nesting sites were conducted under different climate and

soil conditions, and also with other seabird species (Ellis 2005). Preliminary studies within

our study system suggest that soils even on control islands are not extremely nitrogen poor

(Palmborg et al., unpubl), and plant growth may therefore not be strongly nitrogen limited.

Nitrogen is, in contrast to phosphorus, highly volatile. The soil from islands with abandoned

cormorant colonies is therefore not strongly enriched in nitrogen but has however retained

high phosphorus content. This phosphorus rich soil has seemingly enhanced vegetation

growth and aboveground plant biomass. Why this phosphorus effect only cascade up in one

case to higher trophic level is hard to tell but might either be explained by a high predation

pressure or by a lack of phosphorus limitation in terrestrial arthropods. Notice that web-

building spiders had higher densities on abandoned islands and this might have caused the

higher predation pressure. Only future studies that remove also predators along a cormorant

nesting gradient might reveal these indirect effects.

62

Cormorants

Fish

Algae

soil food web

Flies Collembola

Detrivores

Isopoda

•Linyphiidae

•Araneidae

•Tetragnathidae

Lycosidae

Carabidae

Nabidae

Saldidae

Staphylinidae

Parasites Scavengers

Beetles Flies

Herbivores

Plants

Guano

Chironomidae

Coccinelidae

Formicidae

Fig. 7: Preliminary arthropod food web on islands with active cormorant colonies in the archipelago of Stockholm, Sweden. Black lines = mainly signal of marine carbon (enriched δ13C signature) and avian nitrogen (enriched δ15N signature), dashed lines = mainly signature of avian nitrogen (enriched δ15N signature). The size of the line represents the strength of the signal. The thicker the line the stronger is the signal.

Conclusion

Nesting cormorants deposit huge amount of marine nutrient in form of guano on their nesting

islands profit furthermore additional food sources for parasites and scavengers. Avian

nitrogen enters the arthropod food web via three different pathways: plants-

herbivores/detritivores-predators, parasits/scavangers-predators, run-off marine algae-

chironomids-predators. But this avian nitrogen input affects the densities of consumers on

different trophic level only in a few cases. This can be explain by the lack of food and nutrient

limitation of the most consumers due constantly high marine subsidies through shore drifted

algae and chironomids, but also with direct negative habitat effects due to decreased

vegetation cover on active cormorant islands.

63

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Appendix 1: Stable isotope signature of carbon (δ13C) and nitrogen (δ15N) for plant and arthropod communities [mean±SE in the first line of each taxa] on non-seabird islands, islands with an abandoned cormorant colony and islands with an active cormorant colony with a low and a high nest in the archipelago of Stockholm, Sweden. Test statistics from linear mixed effects models (t- and p-values in the second line of each taxa). Sample sizes are provided in parentheses. Values in parenthesis represent sample size. Only significant results (p<0.1) are presented.

taxa non-seabird island abandoned cormorant

island

active cormorant island with a low nest

density

active cormorant island with a high nest

density δ15N

Fucus vesiculosus 5.9±0.9 (60) 4.2±1.6 (24)

6.2±1.6 (24)

16.5±1.6 (24) 6.6 0.000

epiphytic algae 3.8±0.7 (29) 2.1±1.3 (12) 4.5±1.3 (12) 15.9±1.3 (12)

9.4 0.000

ter.plants 1.6±0.9 (85) 15.9±1.8 (29) 8.0 0.000

13.9±1.6 (36) 7.8 0.000

12.9±1.8 (25) 6.1 0.000

Poaceae 3.6±1.4 (19) 21.2±2.8 (6)

6.4 0.000 18.8±3.0 (5) 5.2 0.001

12.2±2.8 (6) 3.1 0.015

herbs 2.7±0.8 (35) 15.5±1.6 (12)

8.3 0.000 12.3±1.5 (13) 6.4 0.000

10.7±2.0 (6) 3.9 0.003

Sorbus aucuparia -2.1±3.0 (7) 15.7±4.8 (5)

3.8 0.013 15.3±4.8 (5) 3.7 0.014

14.7±4.6 (6) 3.6 0.015

Alnus glutinosa 3.6±1.4 (15) 21.2±2.8 (6)

6.4 0.000 18.8±3.0 (7) 5.1 0.001

12.2±2.8 (4) 3.1 0.015

Juniperus communis 1.0±1.2 (9) 10.4±1.9 (6)

4.9 0.016 17.1±2.4 (3) 6.6 0.007

herbivores 4.0±1.1 (33) 20.9±1.7 (28)

9.8 0.000 15.1±1.8 (20) 6.0 0.000

16.2±2.2 (10) 5.6 0.000

Lepidoptera larvae 4.0±2.6 (11) 24.0±4.6 (5)

4.3 0.005 15.4±4.5 (6) 2.5 0.044

15.8±4.5 (6) 2.6 0.040

Cicadina 3.6±1.7 (14) 17.9±3.0 (9)

4.7 0.003 16.0±3.1 (6) 4.0 0.007

16.5±4.0 (3) 3.2 0.019

Heteroptera 5.5±2.8 (6) 21.4±2.8 (13) 4.8 0.018

14.7±4.1 (2) 2.3 0.110

Aphidoidae 1.8±2.8 (2) 17.9±4.9 (1) 3.3 0.080

13.2±3.4 (4) 3.3 0.080

web-building spiders 7.8±0.6 (40) 4.1±1.1 (31) 9.9±1.1 (20)

1.8 0.103 15.9±1.1 (19) 7.1 0.000

Araneidae 7.6±0.7 (24) 6.9±1.3 (15) 9.6±1.3 (9) 16.1±1.4 (5)

6.2 0.000

Linyphiidae 7.3±1.1 (12) 8.0±1.8 (10) 12.8±1.8 (5) 3.0 0.025

15.5±1.8 (6) 4.5 0.004

Tetragnatha 8.0±1.2 (4) 7.1±1.8 (6) 8.2±1.8 (6) 16.0±1.8 (8)

4.4 0.007

Pachygnatha 7.2±1.1 (18) 5.9±2.4 (7) 10.4±2.0 (6) 14.5±2.5 (3) 2.6 0.085

Lycosidae 7.9±0.5 (27) 9.6±1.2 (8) 14.6±0.9 (14)

7.3 0.000 13.5±1.2 (4) 9.7 0.000

69

taxa non-seabird island abandoned cormorant

island

active cormorant island with a low nest

density

active cormorant island with a high nest

density Carabidae 7.3±1.1 (26) 22.8±2.3 (7)

6.2 0.000 18.0±2.0 (11)

5.4 0.000

15.5±2.7 (3) 3.1 0.010

Staphilinidae 4.5±1.1 (17) 15.1±2.7 (3) 4.0 0.002

20.2±2.6 (2) 6.0 0001

Coccinelidae 4.9±0.9 (10) 24.7±2.9 (1)

6.8 0.000 15.3±1.3 (9) 8.1 0.000

16.3±1.5 (5) 7.4 0.000

Formicidae 6.8±0.9 (20) 13.0±1.8 (17) 3.5 0.007

13.1±1.9 (7) 3.3 0.009

18.7±1.8 (14) 6.6 0.000

Nabidae 5.7±1.2 (15) 8.2±2.1 (6) 11.5±2.0 (10) 2.9 0.032

18.8±2.6 (5) 5.1 0.004

Saldidae 5.9±2.0 (6) 8.9±4.0 (5) 18.6±3.2 (2) 3.9 0.029

Chilopoda 6.0±2.9 (2) 16.6±4.1 (2) 22.8±3.4 (6)

brachycerid flies 4.3±3.1 (8) 14.3±4.6 (9) 2.2 0.074

23.0±4.9 (6) 3.8 0.009

24.8±4.9 (6) 4.2 0.006

Isopoda 5.3±1.1 (26) 15.6±2.2 (11) 4.6 0.001

16.2±1.9 (16) 5.6 0.000

21.7±2.3 (7) 7.2 0.000

Collembola 0.3±1.2 (5) 19.9±2.8 (1)

6.5 0.001 16.6±1.9 (3) 8.5 0.000

12.7±2.2 (2) 5.6 0.003

Chironomidae 6.2±1.0 (14) 4.5±1.5 (11) 10.0±1.7 (8)

2.2 0.068 15.0±2.2 (4) 4.0 0.007

Trichoptera 7.7±0.7 (10) 6.4±1.1 (6) 7.9±1.1 (5) 14.8±1.8 (1)

3.8 0.012

Omosita colon 21.4± 0.8 (4) 22.0±0.7 (10)

δ13C

Fucus vesiculosus -19.1±0.7 -19.1±1-3 -19.3±1-3 -18.9±1.3

epiphytic algae -12.0±0.4 -12.8±0.8 -12.7±0.8 -13.0±0.8

ter.plants -29.1±0.3 -290±0.5 -27.7±0.5 -28.1±0.5

herbivores -27.4±0.3 -27.4±0.4 -27.0±0.4 -28.2±0.5

Poaceae -28.6±0.4 -28.7±0.9 -27.7±0.9 -28.6±0.9

herbs -30.2±0.4 -30.3±0.9 -28.9±0.8 -29.6±1.0

Sorbus aucuparia -30.1±0.5 -27.8±0.7 3.3 0.022

-28.0±0.7 3.0 0.031

-27.4±0.7 4.0 0.011

Alnus glutinosa -28.6±0.4 -28.7±0.9 -27.7±0.9 -28.6±0.9

Juniperus communis -27.2±0.2 -25.9±0.4

3.6 0.038 -25.5±0.5

3.7 0.035

Lepidoptera larvae -28.2±0.5 -28.0±0.9 -28.7±0.9 -28.2±0.9 Cicadina -26.8±0.3 -27.6±0.5 -25.8±0.6 -28.4±0.7

-2.1 0.077

Heteroptera -26.6±0.8 -26.9±1.0 -26.3±1.1

Aphidoidae -29.5±1.0 -29.5±1.7 -27.6±1.2

web-building spiders -20.2±0.5 -18.2±0.9 2.2 0.056

-20.3±0.9 -21.1±0.9

70

taxa non-seabird island abandoned cormorant

island

active cormorant island with a low nest

density

active cormorant island with a high nest

density Araneidae -19.9±0.4 -17.9±0.7

2.9 0.020

-20.4±0.7 -21.8±0.8 -2.4 0.042

Linyphiidae -21.1±1.0 -18.4±1-7

-22.2±1.8 -22.1±1.7

Tetragnatha -20.3±1.2 -18.8±1.2

-19.2±1.2 -19.8±1.2

Pachygnatha -19.5±1.1 -18.2±2.3

-21.6±1.8 -21.3±2.3

Lycosidae -21.2±0.5 -19.5±1.2 -21.2±1.0 -24.2±1.2 -2.7 0.036

Carabidae -24.5±0.5 -23.9±1.1

-24.1±0.9 -25.1±1.2

Staphilinidae -22.9±0.4 -22.1±0.9

-21.1±1.5 -22.3±1.1

Coccinelidae -28.3±0.7 -27.0±2.1 -25.6±1.1 2.4 0.046

-26.0±1.4

Nabidae -25.2±1.3 -19.7±2.3 2.4 0.064

-23.5±2.2 -22.1±2.8

Saldidae -23.0±0.9 -21.1±1.7

-19.7±1.4 3.6 0.036

Formicidae -24.5±0.4 -23.3±0.7 -23.4±0.8 -23.0±0.7 2.0 0.076

Chilopoda -24.3±1.3 -21.9±1.9

-22.7±1.6

brachycerid flies -24.3±1.1 -24.3±1.6 -21.8±1.7 -21.0±1.7 2.0 0.094

Isopoda -22.7±0.4 -23.2±0.7 -23.0±0.6 -23.7±0.7

Collembola -25.2±1.3 -29.9±3.0 -22.8±2.0 -23.0±2.7

Chironomidae -20.0±0.7 -18.2±1.1 -21.7±1.2 -19.6±1.6

Trichoptera -20.4±0.9 -18.9±1.5 -18.7±1.6 -19.2±3.0

Omosita colon

-23.1±0.7 -23.4±0.5

71

Appendix 2: Mean chironomid density and weight per 0.7 m2 vegetated island of nine non-seabird islands (=control islands), on three islands with an abandoned cormorant colony and on five islands with an active cormorant colony with a low nest density (<0.4nests/ m2) and two with a high nest density (>0.4nests/ m2). Values for intercept are log-transformed. intercept F R2 R2(%) mean desnity

non-bird island

abandoned island

active island with low nest density

active island with high nest density

0.67±0.36

-0.14±0.72

0.79±0.60

2.44±0.84*

3.2

0.051

39.4

mean weight

non-bird island

abandoned island

active island with low nest density

active island with high nest density

-0.09±0.20

-0.15±0.40

0.37±0.33

1.43±0.46**

3.7

0.037

42.3

Appendix 3: Mean arthropod density per 0.7m2 area island (corrected for vegetation cover) on nine non-seabird islands (=control islands), on three islands with an abandoned cormorant colony and on seven island with an active cormorant colony in the archipelago of Stockholm, Sweden. (intercept: 0=control island, 1=abandoned cormorant islands, 2=active cormorant island). taxa intercept

log(distance to the mainland)

log(area) island category model

Aphidoidae 0: -0.12±0.44 1: -0.41 2:1.58±0.66*

F=3.7 p=0.047 R2=18.1

Lepidoptera

larvae

0: -0.04±0.14 1: 0.75±0.28* 2: 0.90±0.21**

F=9.7 p=0.002 R2=54.9

herbivores beetles 0: 1.16±0.24 1: 0.65±0.49 2: -0.91±0.37*

F=5.7 p=0.014 R2=41.4

fungivores beetles 0: -0.4±0.13 1: 0.87±0.24** 2: 0.41±0.18*

F=5.7 p=0.014 R2=48.0

web-building

spiders

0: 0.83±0.21 1:0.61±0.34* 2:0.04±0.27

F=6.24 p=0.024 log(y+0.5)=intercept+ 0.12log (mainland distance)

F=3.6 p=0.054 F=6.9 p=0.007 R2=47.2

Lycosidae 0: 0.48±0.19 1: 0.07±0.31 2: -0.96±0.24**

F=17.6 p=0.001 log(y+0.5)=intercept+ 0.15g (mainland distance)

F=8.4 p=0.004 F=11.5 p=0.000 R2=69.7

other-spiders log(y+0.5)=-0.04(±0.16) +0.18log (mainland distance)

F=4.8 p=0.042 R2=22.1

Carabidae log(y+0.5)=-033(±0.10) +0.22log(mainland distance)

F=17.7 p=0.001 R2=51.1

Aphidophaga 0: -0.13±0.14 1:-0.01±0.28 2:0.52±0.21*

F=3.5 p=0.055 R2=30.0

72

Appendix 4: Mean arthropod dry-weight per 0.7m2 vegetated island on nine non-seabird islands (=control islands), on three islands with an abandoned cormorant colony and on seven island with an active cormorant colony in the archipelago of Stockholm, Sweden. (intercept: 0=control island, 1=abandoned cormorant islands, 2=active cormorant island). taxa intercept

log(distance to the mainland)

log(area) log(area)*log(mainland dis.)

island category model

ns ns F=6.18 p=0.027 F=3.19 p=0.074

predators 0: 3.64±2.00 1: 0.44±0.22 2: 0.19±0.17 log(y+0.5)=intercept+0.24log(area)*log(mainland dis.)

F=2.8 p=0.063 R2=51.9

ns F=4.9 p=0.042

ns F=7.9 p=0.005

herbivore 0: 0.92±0.69 1: 0.26±0.17 2:0.51±0.13** log(y+0.5)=intercept-0.14log(area)

F=6.9 p=0.004 R2=58.0

ns

ns ns F=4.0 p=0.039

Aphidoidae 0: -0.36±0.37 1: -0.24±0.75 2: 1.44±0.57

F=4.0 p=0.039 R2=33.3

F=8.1 p=0.030

ns ns F=8.1 p=0.004

Lepidoptera larvae

0: 1.17±0.40 1:1.10±0.65 2:2.01+0.51

log(y+0.5)=intercept-0.15log(mainland dis.))

F=7.3 p=0.003 R2=59.3

ns ns ns F=4.1 p=0.037

herbivores beetles

0: -0.52±0.03 1: 0.08±0.06 2: -0.10±0.05

F=4.1 p=0.037 R2=25.1

F=6.5 p=0.021

Ciccadina 0.45±0.19

log(y+0.5)=intercept-0.23log(mainland dis.))

F=6.5 p=0.021 R2=27.6

F=8.8 p=0.010

F=9.7 p=0.002

brachycerid

flies

0:0.17±0.24 1: 0.44±0.39 2:1.35±0.31 log(y+0.5)=intercept-0.10log(mainland dis.))

F=9.4 p=0.001 R2=65.2

F=8.0 p=0.013

F=7.2 p=0.006

saprophagous beetles

0: 1-31±0.99 1: 0.10±0.24 2:0.68±0.18

log(y+0.5)=intercept-0.25log(area)

F=7.5 p=0.003 R2=59.9

F=2.7 p=0.100

Chironomidae 0: -0.09±0.22 1: -0.15±0.44 2: 0.67±0.33

F=2.7 p=0.100 R2=27.6

F=3.1 p=0.072

web-building spiders

0: 1.42±0.29 1: 1.38±0.57 2: 0.09±0.43

F=3.1 p=0.072 R2=28.0

F=9.2 p=0.010

F=3.1 p=0.102

F=4.5 p=0.053

F=4.3 P=0.038

Lycosidae 0: 10.80±5.92 1: -0.00±0.64 2: -1.50±0.51 log(y+0.5)=intercept—5.10log(mainland dis.)-1.03log(area)+0.61

log(mainland dis)*log(area)

F=5.1 p=0.008 R2=66.1

F=5.2 p=0.036

other-spiders -4.14±1.99

log(y+0.5)=itercept+0.51log(area)

F=5.2 p=0.036 R2=23.3

ns ns F=5.12 p=0.039

Carabidae -3.84±2.13

log(y+0.5)=intercept+0.60log(mainland dis.)*log(area)

F=3.0 p=0.062 R2=37.8

F=8.5 p=0.012

F=5.1 p= 0.041

F=14.5 p=0.000

F=14.5 p=0.002

Aphidophaga 0: 6.30±1.69 1: -0.09± 0.18 2: 0.80±0.14 log(y+0.5)=intercept-2.74log(mainland dis.)-0.78log(area)+0.32

log(mainland dis)*log(area)

F=13.0 p=0.000 R2=83.3

parasitic hymenoptera

0:-0.36±0.11 1:0.36±0.22 2:0.34±0.17

F=2.7 p=0.099

F=2.7 p=0.099 R2=25.1

73

74