1. pets
2. birds

The impact of cormorant nesting colonies on
plants and arthropods
Gundula S. Kolb
© Gundula S. Kolb, Stockholm 2010
Cover illustration: N. Småholmen, Bergskäret, Bergskäret, Phalarocorax carb
Photo and illustration: Gundula Kolb and Svante Jerling
ISSN 978-91-7447-147-2
Printed in Sweden by Universitetsservice, US-AB, Stockholm 2010
Distributor: Department of Botany, Stockholm University
Martallen skriver inga skärgårdsdikter
Martallen vet hur dagen varit.
Inget att anteckna
Eller skriva skärgårdsdikter om.
Kvällen kommer som den kommer.
Månen tar sig fram över viken
På det lokala sättet, med vrickåra.
Skrivet suddas genast ut.
Werner Aspenström
Doctoral dissertation
Gundula Kolb
Department of Botany
Stockholm University
SE-106 91 Stockholms Universitet, Sweden
The impact of cormorant nesting colonies on plants and arthropods
Abstract – Seabirds concentrate large amounts of marine nutrients on their nesting
islands. This nutrient input can have large consequences for island food webs and
community structure. The high nutrient load may also cause runoff into
surrounding waters and affect marine communities. In my thesis, I studied the
effect of cormorant nesting colonies on the stoichiometry, abundance, species
richness, and species composition of plants, algae and invertebrates on land and in
costal waters and investigated if differences in the elemental composition or
homeostasis can explain differences in the numerical response among invertebrate
groups. δ15N analysis indicated that ornithogenic nitrogen provided a significant
nitrogen source for plants and arthropods on nesting islands and around high nest
density islands also for brackish algae and invertebrates. Furthermore, nutrient
runoff created a potential feed-back loop to spiders via chironomids. Cormorant
nutrient input changed island vegetation and increased plant P and N content and
epiphytic algae:Fucus ratio, but decreased plant species richness and vegetation
cover. Invertebrates responded indirectly to these qualitative and quantitative
changes in their food source and habitat, but also directly to cormorant subsidies.
However not all taxonomic and feeding groups were affected and responses were
both positive and negative. Differences in the numerical response among
taxonomic groups could not be explained by differences in the level of
homeostasis, since, generally, all invertebrates were strongly homeostatic.
Similarly, consumer nutrient content was a poor predictor for displayed responses.
I conclude that cormorant colonies have strong impacts on island vegetation and
some consumer groups. However, even if they can decrease the species richness of
some organism groups on their nesting islands, they increase the habitat
heterogeneity in an archipelago and thus may increase the regional species
diversity.
Keywords: seabirds, cormorants, islands, nitrogen, phosphorus, plants, arthropods,
δ15N, Baltic Sea, ecological stoichiometry, species richness, species composition,
numeric response
List of papers
This thesis is comprised of a summary and four papers, which are referred to by
their Roman numerals:
I.
Kolb, G. S., Jerling, L. and P. A. Hambäck. 2010. The impact of
cormorants on plant–arthropod food webs on their nesting islands.
Ecosystems 13:353-366
II.
Kolb, G. S., Jerling, L., Essenberg, C. and P.A. Hambäck. The impact of
nesting cormorants on plants and arthropod diversity submitted
III.
Kolb, G. S., Ekholm, J. and P. A. Hambäck. 2010. Effects of seabird
nesting colonies on algae and aquatic invertebrates in costal waters.
Marine Ecology Progress Series accepted in Marine Ecology Progress
Series
IV.
Kolb, G. S. and P. A. Hambäck. Ecological stoichiometry and
homeostasis of plants and invertebrates on and nearby heavily fertilized
cormorant nesting islands manuscript
Paper I is reprinted with the permission from Ecosystems.
Contents
Introduction
 What is this all about? ................................................................................. 11
 Why studying seabird islands ...................................................................... 11
 Seabird as ecosystem engineers................................................................... 13
 The ecology of seabird islands .................................................................... 15
 Ecological stoichiometry ............................................................................. 19
Aims of the thesis.................................................................................................. 22
Material and Methods
 Study system ................................................................................................ 24
 Study organisms........................................................................................... 30
 Sampling ...................................................................................................... 32
 Stable isotope analysis ................................................................................. 33
 Carbon-, nitrogen- and phosphorus analysis ............................................... 35
 Statistics ....................................................................................................... 35
Results and Discussion
 Stable isotope analysis – hypothetical food web (paper I and III) .............. 37
 Effects of nesting cormorants on island ecosystem
 Effect of nesting cormorants on soil chemistry ...................................... 40
 Effect of nesting cormorants on island vegetation (paper I, II and IV) . 42
 Effect of nesting cormorants on island arthropods (paper I and II)...... 43
 Density response (paper I and II)........................................................... 44
 Responses in species richness (paper II) ................................................. 44
 Responses in species composition (paper II) ............................................ 46
 Direct versus indirect effects of nesting cormorants (paper II) ................... 48
 Effects of cormorant nesting colonies on algae and aquatic
invertebrates in coastal waters (paper III)............................................. 52
 My results in the context of other seabird island systems ........................... 54
 Plant and consumer stoichiometry and homeostasis under increase nutrient
loads
 Effects of fertilization on plant and herbivore homeostasis and
herbivore survival and body size – the Lythrum salicaria –
Galerucella system (paper IV)................................................................ 56
 Ecological stoichiometry and homeostasis of plants and invertebrates on
and nearby heavily fertilized cormorant nesting islands (paper IV) ..... 57
Concluding remarks............................................................................................. 60
Further research................................................................................................... 62
Acknowledgement ................................................................................................ 63
References ............................................................................................................. 64
Svensk sammanfattning....................................................................................... 77
Tack ....................................................................................................................... 80
Introduction
What is this all about?
In this thesis I have investigated how cormorant nesting colonies affect terrestrial
plants and brackish algae (hereafter referred to as plants) and terrestrial and
brackish invertebrates on their nesting islands and in near-shore waters around the
islands, in the archipelago of Stockholm, Sweden. Cormorants are fish-eating seabirds that concentrate marine nutrients from a large area on their nesting islands by
depositing guano, carcasses, food scrap and reproduction by-products. Such allochthonous (= from outside the ecosystem) nutrients and energy can have strong
effects on food web and community structure and on population dynamics of the
recipient ecosystem. However, no former study has investigated how the nutrient
and energy inputs of cormorants affect island arthropod communities. This lack of
research is somewhat surprising considering that cormorants in Europe and the US
gain high public interest and are often strongly disliked.
Why study seabird islands?
Islands are important habitats for many species, often endemic or endangered, and
provide, as “model ecosystems”, information on basic ecological and evolutionary
processes (Darwin 1859, see review in Cushman 1995, Vitousek et al. 1995). They
provide perfect study systems due to their limited size and species diversity, their
isolation, clear habitat borders, and worldwide prevalence which allow comparing
the same processes under different abiotic and biotic factors. Not surprisingly,
islands have often been used to study food web interactions (Spiller and Schoener
1994, Polis and Hurd 1995, Polis et al. 1997, Schoener and Spiller 1997), the importance of allochthonous nutrient and energy input (e.g., Polis et al. 2004,
Anderson 1998, 2004, Paetzhold et al. 2008), diversity pattern (e.g., McArthur and
Wilson 1963, Lomolino et al. 2006) and ecosystem functions (Wardle et al .1997,
Jones 2010).
The importance of cross-habitat flows of nutrient, energy and prey for
ecosystem processes was realized by scientists as early as the 1920ties (e.g., Elton
1927, Polis et al. 1997a), but these fluxes were not incorporated in ecological
theories until the 1990ties (Polis et al. 1997b, Power and Huxel 2004). Today it is
commonly accepted that movements of energy, nutrients or prey between systems
are ubiquitous, although the strength of effects from these subsidies vary among
systems (Polis et al. 1997b). It has been proposed that the effects of allochthonous
subsidies on consumer abundances are strongest in recipient systems with a lower
productivity than the donor system (Polis et al. 2004, Barrett et al. 2005). However, strong numeric responses of consumers to subsidies have also been observed
11
in high productive recipient systems (Marczak and Rickardson 2007, Marczak et
al. 2007).
Islands, generally, receive nutrient and energy from the surrounding aquatic
system via four major pathways (Polis et al. 2004) (Fig. 1):
 animals (e.g., seabirds, sea turtles, mammals) which forage in a large
aquatic area, but nest and roost on islands where they deposit huge amounts
of aquatic nutrients and energy (e.g., Huston 1950, Lindeboom 1984,
Anderson and Polis 1999, Mulder et al. 2011)
 shore drifted carrion and detrital algae (Brown and McLachlan 1990; Polis
and Hurd 1996b)
 emerging insects with aquatic larvae (e.g., chironomids) (Nakano and
Murakami 2001, Gratton et al. 2008, Mellbrandt et al. 2010)
 windblown sea foam and spray (Polis et al. 2004)
Seabirds forage in large marine areas and deposit huge amounts of marine
nutrients, mainly in form of guano, on their nesting and roosting islands. Furthermore, seabird islands are not only characterized by the huge allochthonous nutrient
load but also by a strong physical disturbance from the birds (Ellis et al. 2006,
Smith et al. 2011). Through the nutrient input and physical disturbance, nesting
seabirds can affect some of the major factors determining species diversity and
composition (disturbance, productivity, and heterogeneity), limiting population
size (nutrient and energy availability), and regulating food web structures and
dynamics (resource and habitat availability) (Prime 1973, Hart and Horwitz 1991,
Polis et al. 1997, Siemann 1998, Micheli 1999, Mittelbach et al. 2001, Price 2002),
and thus give scientists a great opportunity to study such processes.
The suitability of seabird islands as model ecosystems increases by their worldwide distribution, more than 250 species nest or roost on tens of thousands islands,
in every ocean and several freshwater system and in every climatic region (Croxall
et al. 1984, Mulder et al. 2011). Despite or maybe due to the large cultural and
economic importance of seabird islands for people across the world, many seabird
islands are threatened by human activities (Anderson and Mulder 2011). These
threats include guano mining, introduction of predators, overfishing, pollution, or
simply habitat destruction (Skaggs 1994, Blackburn et al. 2004, Jones et al. 2008,
Anderson and Mulder 2011, Towns et al. 2011). Due to the possible effects of
nesting seabirds on island ecosystems a significant decrease, or an extinction of
seabirds from an island, may change island characteristics and lead to strong
changes in vegetation structure, species composition and ecosystem function
(Wardle et al. 1997, Maron et al. 2006, Towns et al. 2009). In order to predict the
consequences of the seabird loss for island ecosystem, one needs to understand
nutrient cycles, food web structures and ecosystem processes on seabird islands.
12
Figure 1. Marine nutrient input to terrestrial island ecosystems.
Seabird as ecosystem engineers
Birds that spend most of their life at sea are commonly called ´seabirds`, but the
use of this term is highly discussed among biologists (Smith et al 2011). Generally,
the term seabird includes the orders Sphenisciformes, Procellariiformes and
Pelecaniformes (Gaston 2004). Totally, 222 marine bird species feed exclusively
on marine food and nest near the sea, and 92 additional species are partially marine
or freshwater species (Smith et al. 2011). Seabirds are wide-ranging pelagic and
near-shore predators, foraging in areas as large as several km2, feeding across
several trophic levels, from zooplankton to fish. Many seabirds are so called
´ecosystem engineers`, altering their nesting islands physically via their nesting
activities and chemically via their deposition of marine nutrients (Jones et al. 1994,
Smith et al. 2011). The strength of seabird impacts on the ecosystem of their
nesting islands is strongly influenced by the seabird identity, which affect the time
span of birds occupancy, the size of the colony, the nest density, the size of the
bird and thus the guano volume per bird, guano nutrient content, and nesting typ.
The time span of occupancy can vary from 32 days once per year, to year around
in the tropics. 98% of all seabird species breed in colonies (Rolland et al. 1998)
including a few up to 10 million nests. The size of the colony will directly affect
the total nutrient input to the islands, whereas nest density will affect nutrient load
per square meter. Seabirds transport marine-derived nutrients to their nesting and
roosting islands by foraging at sea and defecating on land, as well as dropping
food items, losing feathers and providing egg shell (Barrett et al. 2005). Marine
nutrients and carbon are also added to the island ecosystem when birds die
(Sánchez-Piñero and Polis 2000). However, guano is by far the most important
nutrient subsidy on seabird islands (López-Victoria et al. 2009). For example, on
13
Malpelo Islands, Colombia, 40,000 breeding pairs of Nazca boody (Sula granti)
were estimated to deposit 171.6 t marine nutrients during one breeding season (160
d), of which 170 t was guano (López-Victoria et al. 2009). Such huge ornithogenic
nutrient loads have also been reported from the Rottnest Islands, Australia, where
11,700 wedge-tailed shearwaters (Puffinus pacificus) were estimated to deposit
234 kg ha-1per year.
Guano is a complex mixture of undigested food residue and metabolic waste
products, including uric acid as one of the main metabolic waste products (Bird et
al. 2008). Fresh guano contains approximately 60% water, 7.3% nitrogen and
1.5% phosphorus (Smith and Johnson 1995). However, the exact nutrient
composition differs between species and habitats depending on bird metabolism
and food composition (Hahn et al. 2007, Smith et al. 2011). For example, dried
cormorant guano from a French lake has been reported to contain 3.3% N and
14.3% P (Marion et al. 1994), whereas the cormorant guano from a Japanese lake
was estimated to contain about 10.1% N and 9.2% P (Osono et al. 2002). The
principal form of N in fresh seabird guano is uric acid, accounting for 50-80% of
guano N. The other major N-containing compound in guano is NH4+ making up 840%. Amino acid and proteins account only for > 8% of guano N (Lindeboom
1884, Schmidt 2004). After guano deposition on the island, ammonia volatilizes
rapidly from the uric acid and cause N - losses between 25-80% of total guano-N
and, as later discussed, an increase in δ15N signature in the remaining guano
(Lindeboom 1884, Smith and Johnson 1995). The P in fresh guano-P consists of
54.4% PO4 (Lindeboom 1884, Smith and Johnson 1995).
The second greatest factor that characterizes seabirds as ecosystem engineers is
physical disturbance. The strength of this disturbance is strongly dependent on the
nesting type and seabird behavior. Generally, four types of seabird nests can be
found: surface nests, tree nests, crevice and cavity nests, and burrows. The
strongest physical disturbance is caused by burrowing seabirds, affecting soil
structure and damaging vegetation by removing twigs and leaves and damaging
roots (Smith et al. 2011). Surface and tree nesters, like cormorants, can also
strongly violate the vegetation. Surface nesters disturb the ground surrounding of
their nests by trampling, whereas tree nesters physically damage trees by breaking
branches and removing leaves to line their nests (Hobara et al. 2001). Furthermore,
cormorants were also observed to eliminate recruitment of new seedlings (Ishida
1996, Hebert et al. 2005).
14
Pathways and expected effects of cormorant subsidies
Cormorant subsidies
Pathway of cormorant subsidies (δ15N)
Effects of cormorant on density and
diversity (= species richness)
Cormorants
carcasses
↑ increase, ↓ decrease
Predators
N and P rich Guano
Scavengers ↑ density
↑ diversity
Vegetation:
Herbivores
↑ density
? diversity
↑ density
↑ diversity
Detritivores
↑ density
↑ diversity
Chironomidae ↑ density
↑ N and P, ↑ biomass,
↓ species richness
Marine algae
Soil:
↑ N and P
↑ epiphyte biomass
↑N and P ↓pH
↓ moisture
Grazer
N and P rich run-off
↑ density
Water: ↑ N and P
Figure 2. Conceptual model for the effects of nesting seabirds on islands ecosystem.
The ecology of seabird islands
The former paragraph described the role of seabirds as ecosystem engineers. Now
I will discuss the consequences the engineering can have for the island ecosystems
(see conceptual model in Fig. 2). It has been show that seabirds can largely affect
soils and vegetation on their nesting islands through nutrient deposition and
physical disturbance (e.g., Gillham 1961, Burger et al. 1978, Sobey and
Kenworthy 1979, García et al. 2002, see review by Ellis 2005, Wait et al. 2005,
Fukami et al. 2006, see metaanalysis Mulder et al. 2011). The large majority of
studies comparing nutrient content in soils from seabird colonies with the nutrient
content in soils at a distance from colonies found increase soil N and P contents
within the colonies (e.g., Ishizuka 1966, Burger et al. 1978, Mizutani and Wade
1988, Polis and Hurd 1996, see review by Ellis 2005, Hobara et al. 2005, Wait et
al. 2005, see metaanalysis by Mulder et al. 2011). Furthermore, stable isotope
analysis of N has indicated a considerable input of marine-derived N to the soils of
seabird islands (Mizutani et al. 1986, Erskine et al. 1998, García et al. 2002,
Fukami et al. 2006, Maron et al. 2006). Accordingly, the enriched δ15N signature
of plants on seabird islands and their increased N and P content demonstrate that
marine nutrients are taken up by island vegetation and thus enters the island food
15
webs (Erskine et al. 1998, Wainwright et al. 1998, Anderson and Polis 1999,
García et al. 2002, Ellis et al. 2006, Fukami et al. 2006, Maron et al. 2006).
However, even if the vast majority of studies described increased N and P content
of soils and plants in seabird colonies, the strength of the nutrient increase varied
strongly among studies. The increased nutrient content in the soils of seabird
islands is expected not only to increase plant nutrient content but also to change
plant species composition, plant species richness, and primary productivity.
Fertilization experiments show that high nutrient loads decrease plant species
richness, change species composition towards a few fast growing, nutrient tolerant
species with high fecundity, and increase primary productivity (Tilman 1987,
Wedin and Tilman 1996, Siemann 1998, Haddad et al. 2000). However, island
vegetation is expected not only to respond to ornithogenic nutrient input, but also
to the physical disturbance by seabird nesting activity. Strong physical disturbance
should decrease plant species richness and change species composition towards
taxa that exhibit high resilience (Connell 1978), whereas an intermediate level of
disturbance (= low nest density) may increase plant species richness (Connell
1978). Primary productivity may similarly decrease under strong disturbance.
Thus, the total impact of seabirds might be regulated by the balance of nutrient
addition and physical disturbance (Mulder et al. 2011). Accordingly, Ellis (2005)
found that the number of plant species is lower on seabird islands than on similar
islands without seabirds. Furthermore, the plant species composition differed
significantly between seabird and non-seabird islands. The families Apiaceae,
Brassicaceae, Chenopodiaceae, Poaceae and Solanaceae were most frequent and
species-rich on seabird islands, whereas Gentianaceae and Orchidaceae were most
frequent and species-rich on non-seabird islands (Ellis et al. 2011). Primary
productivity is difficult to measure in the field and therefore, has rarely been
studied on seabird islands. In a couple of studies on seabird islands, aboveground
plant biomass has been used as estimate for primary productivity indicating that
the effect of nesting seabird on plant productivity differ by archipelago (Anderson
et al. 2008, Maron et al. 2008, Wardle et al. 2007).
In their role as ´ecosystem engineers` seabirds not only affect island vegetation
but also island consumers (e.g., Polis and Hurd 1995, Barrett et al. 2005, Towns et
al. 2009, see review by Kolb et al. 2011), primarily via their role as vectors of marine nutrients onto islands and as physical modifiers of island soils and vegetation.
Through either role seabirds alter the quantity and quality of food and habitat
resources of island consumers. As nutrient vectors, they subsidize the diet of
consumers on different trophic levels. This effect has been shown with stable
isotope analysis; consumers from different seabird islands systems, including
amphipods, insects, spiders, snails, lizards, geckos, and rodents have been found to
be enriched in 15N and thus included seabird-derived N in their diet (SánchezPiñero and Polis 2000, Stapp and Polis 2003, Wolfe et al. 2004, Barrett et al. 2005,
Fukami et al. 2006, Maron et al. 2006, Hawke and Clark 2010, Kolb et al. 2011).
Nitrogen and phosphorus from guano is taken up by plants which are then
consumed by herbivores, detritivores, and their predators (Sánchez-Piñero and
Polis 2000, Barrett et al. 2005, Fukami et al. 2006). Guano itself can be consumed
16
directly by some invertebrates (Sánchez-Piñero and Polis 2000). Eggs and chicks
are prey for larger predators (e.g., snakes, hawks, rodents), and, together with adult
carcasses and food scraps, provide resources for scavenging insects (Polis and
Hurd 1996, Sánchez-Piñero and Polis 2000). Live seabirds also support several
ectoparasites, which can become prey for arthropod predators (Polis and Hurd
1995). The multiple pathways by which seabirds “subsidize” the diet of island
consumers can generate different direct and indirect responses in island consumer
groups, including changes in population sizes, fitness, survival and species
richness (e.g., Iason et al. 1986, Wolfe et al. 2004, Polis and Hurd et al. 1995,
Towns et al. 2009). Increased abundance has been reported from rotifers,
enchytraeids, nematodes, snails, amphipods, several orders of insects (including all
major trophic groups), chilopods, mites, spiders, and lizards (Onuf et al. 1977,
Iason et al. 1986, Polis and Hurd 1995, 1996, Ryan and Watkins 1989, Markwell
and Daugherty 2002, Oregeas et al. 2003, Barrett et al. 2005, Fukami et al. 2006,
Sinclair and Chown 2006, Towns et al. 2009). However, not all consumers
respond with increased abundances on seabird islands, some showed no response,
such as soil invertebrates in Antarctica (Sinclair 2001) and 11 of 19 investigated
litter-invertebrates in New Zealand (Towns et al. 2009) and in one case – herbivorous beetles in a gull colony on a French Mediterranean island (Oregeas et al.
2003) – a negative. Different consumer responses may be partly due to differences
in species traits, particularly traits known to affect consumer responses to nutrient
input. A further explanation for the absence of positive numeric response might be
the fact that food webs are rarely simple and linear. Even though seabird effects
are primary bottom-up effects, top-down forces will likely bias the overall results
(Hunter and Price 1992) and in some cases top-down effects can overwhelm the
benefits of an primary consumers and cause a zero or even negative consumer
response (Fukami et al. 2006).
Furthermore, seabird induced changes in soil and vegetation may affect the
habitat quality for some consumers negatively and thus again overwhelm the
bottom-up benefits from an increased nutrient availability (Oregas et al. 2003).
The effects of nesting cormorants on resource availability and habitat quality
might not only affect consumer abundance but also consumer species richness and
composition (Towns et al. 2009, Oregas et al. 2003). For examples, seabirds can
change several characters of island vegetation with consequences for island
consumers. Increased plant nutrient content and biomass and decreased plant
species richness, concentrate the resources in the vegetation and increase the tissue
quality for herbivores and thus may, assuming bottom-up control, directly increase
herbivore and detritivore abundance and indirectly the abundance of predators
(Root 1973, Mattson 1980, Kyto et al.1996, Siemann 1998, Haddad et al. 2000,
Barrett et al. 2005). Similar to the positive effect on consumer abundance, higher
plant nutrient content and productivity may also increase consumer species
richness (Mattson 1980, Waide et al. 1999, Haddad et al. 2000, Mittelbach et al.
2001). In contrast, lower plant species richness should, according to the habitat
heterogeneity hypothesis, support fewer consumer species than higher plant
17
species richness (MacArthur and MacArthur 1961, Siemann et al. 1998, Haddad et
al. 2000, Hart and Horwitz 1991).
Summarizing, seabird islands seem, generally, to be resource-driven systems,
and seabird-derived subsidies have mostly positive effects on the abundance
consumer groups, while the effect on species richness remains widely unknown.
Effects of nesting seabirds are not limited to the terrestrial systems but also include
adjacent aquatic systems (see review by Young et al. 2011). Seabirds can affect
marine and freshwater systems both as predators via ´top-down effects` and as
nutrient vectors via ´bottom-up effects`. Top-down effects have been reported
from the intertidal systems where seabirds prey on limpets, snails and crabs (Ellis
et al. 2007, Wootton 1992, Kurle et al. 2008), whereas it is debated to what extent
fish-eating seabirds affect their prey populations (Draulans 1988). Most seabirds
forage in large marine areas and share their prey with other predators (e.g., fishery,
mammals, and predatory fishes) which makes it difficult to study the seabird effect
on prey abundance. However, studies on freshwater systems demonstrate that
waterbirds, shorebirds, and seabirds can contribute significant amounts of nutrients
into the water column and sediments, and can stimulate primary and secondary
productivity (e.g., Blais et al. 2005, Hahn et al. 2007, Keatltey et al. 2009, see
review by Young et al. 2011). Less clarity exists on the types and magnitudes of
seabird effects on marine systems, because of the huge variation in ecosystems
structure and sampling method used. However, most studies indicate similar, even
though weaker, effects than in freshwater systems (Golovkin 1967, Onuf et al.
1977, Bosman et al. 1986, Bosman and Hockey 1988, Litter et al. 1991, Wootton
1991). Nutrients from guano can enter water bodies near bird colonies in four
ways. Firstly, birds directly deposit guano into the water (Wainright et al. 1998).
Secondly, guano runs off from bird colonies into surrounding water bodies
(Golovkin and Garkavaya 1975, Smith and Johnson 1995). The amount of nutrient
runoff from land depends on nest density, climate, vegetation and habitat structure
(Branvold et al. 1976, Smith and Johnson, Loder et al. 1996). Thirdly, guano
enters marine systems via leaching of nitrogen into ground water, following
subsequent dispersal during tidal oscillation (Smith and Johnson 1995). Finally,
guano enters marine systems after volatilization to ammonia, which then dissolves
in rain. Increased nutrient concentrations in the water column nearby seabird
colonies have been reported from several systems, including rock pools, bays,
coastal lagoons, coastal areas, and islands (Golovkin and Garkavaya 1975, Bedard
et al. 1980, Bosman et al. 1986, Lapointe et al. 1992), but only one study
combined nutrient content analysis with stable isotope analysis and thus was able
to determine the actual role of guano within the systems. Increased water nutrient
content should, due to their N or P limitation increase productivity of marine
primary producers (Elser et al. 2007). Accordingly, algae and vascular plants near
seabird colonies were shown to have increased abundances, growth rates or
nutrient content (Golovkin 1967, Onuf et al. 1977, Bosman et al. 1986, Bosman
and Hockey 1988, Litter et al. 1991, but see Wootton 1991). These changes in the
primary producers can affect aquatic consumers via bottom-up forces and both in18
crease (Zelickman and Golovkin 1972, Onuf et al. 1977, Bosman and Hockey
1986, Palomo et al. 1999) and decrease (Wootton 1991) consumer abundance.
To summarize and conclude, nesting seabirds can have strong effects on islands
ecosystems, both on land and in the water. However, there is a huge variation
between systems depending on biotic and abiotic factors like size of seabird
colony, nesting density, climate, habitat structure, ecosystem nutrient status, and
community structure. Far more studies are needed to develop good prediction
about the effects of nesting seabirds on island ecosystems.
Ecological stoichiometry
In order to understand seabird impacts on island communities and to predict
seabird effects on community structure and species composition it may be
worthwhile to look closer on species traits assumed to affect organisms’ responses
to nutrient input. An organism`s response to increased nutrient content in its
resource should be dependent on its nutrient requirements for survival, growth and
reproduction. Phytophagous insects generally face the problem of large mismatch
in nutrient content between their body tissue and plant tissue; plants content in
average 10-20 times lower N and P than herbivores (McNeill and Southwood
1978, Mattson 1980, Elser et al. 2000). This unbalanced elemental composition
between plants and consumers is thought to cause nutrient limitation in herbivores
and detritivores (White 1993, Cross et al. 2003) and to critically influence
herbivore survival, growth, and fecundity (Slansky and Feeny 1977, Mattson 1980,
White 1993, Joenern and Behmer 1997, Wheeler and Halpern 1999). Therefore,
increased plant nutrient content (as on seabird islands) should increase survival,
growth, and reproduction rates of primary consumers and their abundance.
Consumers on higher trophic levels may similarly to herbivores also feed on diets
lower in nitrogen content than themselves (Fagan et al. 2002). Increased plant
nutrient content therefore may cascade up to higher trophic levels and increase
consumer abundances via increased prey abundance or prey nutrient content
(Mayntz and Toft 2001, Hunter 2003, Raubenheimer and Simpson 2004).
However, consumer response to increased nutrient availability may differ
among species due to differences in nutrient demand. The nutrient demand of a
given taxa is determined by its metabolism, structural design, specific growth rate
and is reflected in its elemental composition (Elser et al. 1996, Elsner et al. 2000,
2003, Sterner and Elsner 2002). The growth rate hypothesis (GRH) propose that
differences in organismal P content are caused by differential allocation to P-rich
ribosomal RNA in order to meet the protein synthesis demands of rapid growth
rates (Elser et al. 2000a,b, Sterner and Elser 2002). That is, fast growing species
have higher P body content and thus higher P demands and are more sensitive to P
limitation than slow growing species (Urabe and Watanable 1992, Sterner and
Elser 2002, Urabe et al. 2002). In nutrient rich environment, like seabird islands,
therefore fast growing taxa with high N:C and P:C ratios may be more successful
19
and thus dominant over consumers with low ratios whereas the opposite may occur
in nutrient poor environments (Urabe and Watanable 1992, Urabe et al. 2002).
Accordingly, differences in the elemental ratios among consumer groups may
explain differences in their numeric response to nutrient content. Nutrient rich
consumers should be more favoured by increased resource nutrient content and
display stronger numeric response on seabird islands than nutrient poor consumers.
A branch of ecology studying the relationship between elemental ratios,
namely carbon (C), nitrogen (N) and phosphorus (P), of organisms and ecological
processes and interactions is called ecological stoichiometry. Ecological
stoichiometry is defined as the study of the balance of multiple chemical substances (elements) and sometimes energy in biological processes of living systems
and in ecological interactions (Sterner and Elser 2002). It simplifies natural
complexity to a limit set of chemical parameters and applies the law of definite
proportion and conservation of mass, in order to increase the understanding of
factors limiting growth, abundance, and distribution of organismal ecological
stoichiometry (Sterner and Elser 2002). Based on these principles, ecological
stoichiometry explains and predicts biological processes, food web structures, and
community compositions. Thus, stoichiometric homeostasis, the physiological
regulation of organism elemental composition relative to their external world, is a
key concept in ecological stoichiometry (Kooijman 1995, Sterner and Elser 2002).
Organisms with homeostasis can keep the chemical composition of their body
constant, independent of the chemical composition of their food source or the
environment (Kooijman 1995). This homeostasis can be maintained by food
selection and physiological regulation of elemental uptake, assimilation, or
excretion (Logan et al. 2002, Anderson et al. 2005, reviewed by Frost et al. 2005).
Heterotrophs (animals) are commonly seen to be more homeostatic than autotrophs (plants) (Sterner and Elser 2002, Persson et al. 2010). Based on differences
in physiology; autotrophs house, in contrast to heterotrophs, large central vacuoles
in which they can store highly concentrated nutrients (e.g., N and P) or nutrientfree organic matter (e.g., sugars). However, during the last decade, the generality
of strict homeostasis has been questioned and several studies indicate that the
C:N:P ratio of some heterotroph species can vary in dependence of resource
nutrient content (e.g., DeMott 2003, Mulder and Bowden 2007, Mulder and Elser
2009, Small and Pringle 2010, reviewed by Persson et al. 2010). Plastic organisms
may be better adapted and more successful to variable environments than strict
homeostatic organisms; because they store nutrients for later growth (Sterner and
Schwalbach 2001, Raubenheimer and Jones 2006) and can, when consuming a
nutrient poor diet, increase their nutrient use efficiency by adding a lower concentration of nutrients to new tissue (Elser et al. 2003). Thus plastic organisms may be
able to buffer variations in nutrient supply and respond less to variation in nutrient
availability (e.g., cormorant versus reference islands). The degree to which
organisms are homeostatic may affect ecological interactions and, furthermore,
influence the magnitude and nature of their ecological impact (Elser and Urabe
1999, Kay et al. 2002, Grover 2003, Mulder and Bowden 2007), e.g., strict homeo20
stasis may cause a disproportional depletion of resources with scarce elements and
increase recycling rates of other elements (Vanni 2002).
However, despite these important consequences on both individual and
community level and strongly increased anthropogenic nutrient load little research
has been done on the level of elemental homeostasis in heterotrophs others than
zooplankton (see review Persson et al. 2010).
21
Aims of the thesis
The overall aim of this thesis was to investigate and understand how cormorant
colonies affect terrestrial plants, brackish algae and invertebrate communities on
and nearby their nesting islands (Fig. 3).
1) I analyzed the food web structure using stable isotope, particularly the relative
use of marine versus terrestrial C and N, on and off islands with cormorant
nesting colonies and compared the food web structure with that on reference
islands (paper I).
2) I investigated the consequences of the high N and P input by nesting
cormorants on island vegetation: aboveground biomass, species richness,
species composition, and N and P content (paper I and II).
3) I assumed that changes on primary producers have consequences on higher
trophic levels and a further question was thus how cormorants directly and
indirectly affect island consumer abundance, species richness and species
composition (paper I and II). Do taxonomic and feeding groups differ in their
responses to nesting cormorants (paper I and II)? Which consumer groups
respond directly to the cormorants and which groups respond to changes in the
vegetation structure (paper II)?
4) Stable isotope analysis indicated that ornithogenic N also enters brackish algae
in the near-shore waters of cormorant nesting islands. Thus I investigated
how cormorants affected near-shore algae, the algae N and P content, and the
abundance and biomass of marine invertebrate grazers (paper III)?
5) Differences in the response of consumer groups to cormorant colonies may be
caused by differences in consumer nutrient demands and elemental
homeostasis. Therefore, I investigated the N:C, P:C, and N:P content of
primary producers and consumers on and around cormorant islands and tested
for their elemental homeostasis. We tested following hypothesis (paper IV):
 Nutrient rich taxa may be more favored by the high nutrient availability on
cormorant islands than nutrient-poor taxa
 Autotrophs are more homeostatically plastic than heterotrophs.
 Strictly homeostatic consumers may show a stronger numerical response to
cormorant nutrient input than more plastic consumers.
22
Water
Soil
Changes in
• Microflora/fauna
• Nutrient content
• ph
• Moisture
• Structure
Paper IV
Cormorant nesting colony
Guano
Carcasses
Eggshells, Feathers
Food scrap
Possible responses
Paper I
Arthropods
Terrestrial vegetation
Changes in
• Productivity/Biomass
• Species richness
• Species composition
• Tissue quality
• Seed production
• Growth rate
• Population dynamics
Possible responses
Paper III
Changes in
• Abundance
• Biomass
• Species richness
• Species composition
• Tissue quality
• Fitness
• Growth rate
• Population dynamics
Paper I
Paper II
Paper IV
Changes in
• Biomass
• Abundance
• Species richness
• Species composition
• Tissue quality
• Fitness
• Growth rate
• Population dynamics
Possible responses
Possible responses
Changes in
• Productivity
• Species richness
• Species composition
• Epiphytic algae: Fucus
ratio
• Tissue quality
• Growth rate
• Population dynamics
Changes in
• N and P content
Kappa
Invertebrtaes
Brackish algae
Figure 3. Possible responses of soil, water, terrestrial plants, brackish algae, and terrestrial and
brackish invertebrates to cormorant nesting colonies. Marked are responses studied in this thesis.
23
Methods
Study system
Figure 4. Location of the islands in Stockholm archipelago, Sweden studied in thesis. For
further information see Table 1.
The studies in this thesis were conducted on and around 27 islands in the archipelago of Stockholm, Sweden (Fig. 4). The archipelago includes about 24,000
large and small islands spread over an area more than 35,000 km2. The archipelago
is part of the Precambrium peneplane. It is subject to isostatic rebound after the
retreat of the last icesheet, at a current rate of 0.47 cm/year (Ericson and
Wallentinus 1977). The bedrock consists of granite-gneiss, on the islands mostly
covered with a very thin soil layer. The yearly precipitation averages 518 mm; the
mean temperature is 6.1°C.
At the latitude of Stockholm the archipelago stretches about 100 km out to the
east. The inner archipelago is characterized by large and small islands covered by
pine (Pinus sylvestris) and spruce (Picea abies) forest harboring forest species
(e.g., Vaccinium myrtillus, Convallaria majalis and Polygonatum odoratum) and
some agricultural land. The central archipelago includes many small islands
vegetated by deciduous trees (Alnus glutinosa and Sorbus aucuparia). Common
are shrubs (Juniperus communis, Rosa canina, and Rubus idaeus), herbs, grasses
and bare rocks. The outer archipelago consists of groups of sparsely vegetated
24
small islands and skerries sprinkled in wide open waters. The most widespread
herbs along the shore and on non forested islands are Atriplex spp, Glaux martima,
Filipendula ulmaria, Valeriana salina, Lythrum salicaria, Tanacetum vulgare,
Veronica longifolia, Viola tricolor, Allium schoenoprasum, Sedum acre, Sedum
telephium and the grasses Phragmites australis, Phalaris arundinacea, Festuca
pratensis, and Deschampsia flexuosa. Until the 1950ties, most islands in the
archipelago were used for farming and livestock. Today, the majority of buildings
on the islands are summer houses and the archipelago is frequently visited by
tourists for boating, swimming and sun bathing.
The water in the Baltic Sea is brackish with a salinity varying between 5.5 and
7 psu in the archipelago of Stockholm. The low salinity enables only a few marine
and freshwater species to occur in the Baltic Sea. The vegetation on hard bottom of
the upper sublittoral zone (0.5-1m) is dominated by filamentous algae and the
species composition varies between seasons. In summer Cladophora glomerata
often dominates (Kautsky et al. 2000). Below C. glomerata, the marine brown
algae Fucus vesiculosus (bladderwrack) (hereafter Fucus) usually dominates.
Below the Fucus belt, marine red algae take over. Fucus is a key species in the
Baltic Sea, supporting about 30 species of macrofauna and epiphytes and
providing spawning, foraging, and nursery areas for fish (Kautsky et al. 1992,
2000). On soft bottoms aquatic phanerogams and charophytes grow. Species
composition varies with depth and bottom characteristics. The water body in the
inner archipelago is sheltered from the open sea and consists of shallow bays and
fjords. The inner waters are strongly influenced by freshwater and land-based
substances from stream and coastal catchments. During January and February
large parts of the inner archipelago are often covered by ice. The outer archipelago
is very exposed to wind and waves, especially in the east.
Eutrophication is one of the major environmental problems in the Baltic Sea,
especially in coastal regions, and the main nitrogen sources are rivers and
atmospheric deposition (Elmgren 2001, Voss et al. 2006). The main nutrient inputs
to the archipelago are discharges from sewage treatment plants, the outflow from
Lake Mälaren in central Stockholm, and the atmospheric deposition on the surface.
The nutrient load to the archipelago decreases from the inner to the outer
archipelago (Aneer and Arvidsson 2003). In the 1990s, discharges from sewage
treatment plants and the outflow of Lake Mälaren contributed an annual load of
5,960t nitrogen and 10t phosphorus to the inner archipelago (Stockholm Water
Company 2004 in Hill and Wallström 2005). According to Swedish water-quality
criteria (Swedish Environmental Protection Agency 1999 in Hill and Wallström
2005), the nutrient concentrations in the surface water were categorized to be
"high" to "very high" in the inner waters and "low" to "very low" in the outer
waters. Such nutrient concentrations cause extensive blooms of Cyanobacteria in
the inner archipelago, and a decrease in the depth distribution of Fucus. In many
parts of the archipelago, eutrophication has caused anoxic conditions on deep
bottoms and killed macrofauna. Eutrophication may have caused increased
densities of pikeperch (Sander lucioperca) and smaller catches of whitefish
(Coregonus spp.) (Hansson and Rudstam 1990).
25
Large colonies of seabirds exist in the outer archipelago. About 170,000-180,000
pairs of seabirds breed in the Stockholm archipelago (Kautsky et al. 2000). Great
cormorants not only nest in the outer archipelago but also in the center and inner
archipelago.
For our studies, we chose eleven islands with active and three with abandoned
cormorant colonies and 13 reference islands without nesting cormorants (Tab 1,
Figs. 4 and 5). This includes about 50% of all cormorant colonies of the archipelago. The islands differ in size (0.3 to 2.7 ha), distance from mainland (0.1 to 18
km), wave exposure, and vegetation type (forest or open grassland). The nest
densities in the active cormorant colonies ranged from 0.007 to 0.070 nest/m²
(2008) and the time span since colonization was two to 12 years (2009).
Cormorants are sensitive to human disturbance and colonies are typically established on islands with limited human activity. To reduce the probability of confounding results we chose reference islands in the same range of size and distance
to the mainland and with similar vegetation structures as the cormorant islands.
26
Figure 5. Cormorant nesting islands in Stockholm archipelago, Sweden. (A) Active cormorant
island with high nest density (N. Småholmen), (B) Active cormorant island with low nest
density (Bergskäret), and (C) Island with an abandoned cormorant nesting colony (S. Halmören).
27
Table 1. Summary of the 27 islands studied.
Island
Area
(ha)
Wave
exposure
Nest
density/
m2
2007
(2008)
Mean nest density/m2
2004 2007
20032008
20062009
Time span
of active
colonization
Vegetation
Sp/m2
E
Sp
bio
vegco
Arthropod sampling
D-Vac
2007
pit fall
2009
sweepnet
2008
Fucus
sampling
Abandoned Cormorant Islands
Kattören*3
0.326
0
0
0
0
0
1997 – 00
Y
Y
Y
N
N
N
St.Halmören*2
0.809
A 51374
B 50072
0
0.012
0.007
0
2002 – 05
Y
Y
Y
Y
Y
Y
St.Träskär*2
1.573
A 52051
B 51900
0
0.005
0.002
0
1996 – 05
Y
Y
Y
Y
Y
Y
(0.070)
0.006
0.023
0.032
2007 – 09
Y
N
N
N
Y
N
Active Cormorant Islands
Alörarna *1
0.233
Marskärskobben*1
0.716
A 19060
B 18821
0.025
(0.030)
0.018
0.023
0.025
2003 – 09
Y
Y
Y
Y
Y
Y
N.Småholmen*4
0.855
A 6785
B 7738
0.063
(0.052)
0.054
0.058
0.057
2000 – 09
Y
Y
Y
Y
Y
Y
S.Småholmen*4
0.701
0.027
0.024
0.026
0.028
1998 – 09
Y
Y
Y
Y
N
N
0.039
(0.052)
0.029
0.042
0.051
2003 – 09
Y
Y
Y
Y
Y
Y
0.017
0.006
0.015
0.024
n.a.– 09
Y
Y
Y
Y
N
N
0.029
(0.028)
0.026
0.027
0.030
1998 – 09
Y
Y
Y
Y
Y
Y
0.008
0.020
0.021
0.020
2002 – 09
Y*
Y
Y
N
N
N
N.Ryssmasterna*4
0.322
S.Ryssmasterna*4
0.369
Bergskäret*5
2.273
Delö*6
0.170
A 9524
B 9202
A 16834
B 19002
Skraken*7
1.688
A 8846
B 8613
Våmkubben*8
1.051
A 340983
B 340983
(0.041)
N
N
N
N
N
Y
Fälöv*8
1.431
A 181913
B 180627
(0.034)
N
N
N
N
N
Y
0.329
A 21710
Y
Y
Y
Y
Y
Y
(0.024)
N
N
N
N
N
Y
Reference Islands
Fårörarna*1
B 21710
Norröra*2
1.248
Ägglösen*2
1.736
V.Mellgrund*2
0.389
Ljusstaken*3
0.553
Hannasholmen*4
0.774
S. Nickösö*4
0.521
N. Nickösö*4
0.520
Mjölingsören*5
2.729
Ostkanten*6
0.234
Fredagen*7
1.803
Rödkläppen*8
Skorvan*8
Y
Y
Y
N
N
N
A 71649
B 77045
Y
Y
Y
Y
Y
Y
A 50567
B 50393
Y
Y
Y
Y
Y
Y
Y
Y
Y
N
N
N
A 7616
B 8023
Y
Y
Y
Y
Y
Y
A 9793
B 9783
Y
Y
Y
Y
Y
Y
N
N
N
Y
N
N
Y
Y
Y
Y
Y
Y
Y*
Y
Y
N
N
N
A 11073
B 10883
N
N
N
N
N
Y
1.285
A 382085
B388320
N
N
N
N
N
Y
1.688
A 297421
B 298047
N
N
N
N
N
Y
A 17361
B 17361
Note: Locations are shown in Fig. 1. : Sp: total plant species richness, Sp/m2: mean species richness/m2, E: evenness, bio: aboveground plant biomass (g/0.0625 m2), vegc:
vegetation cover, Y: yes, N: no. * Total plant species number on these islands were estimated with help of morphospecies for grasses and were not included in plant species
richness analysis. Wave exposure was calculated as effective fetch (distance of free water) in 16 directions for both Fucus sample sides (A and B) per islands with the help
of the program WaveImpact (Isæus 2004). Variables not shown in the table have not been used for analysis.
Study organisms
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
occurring in the Stockholm archipelago. Great cormorants live in colonies of up to
10,000 pairs (nesting colonies) or 12,000 individuals (roosts) (Carss 2002). They
breed and roost in trees, on bare soil or rocks and in reed beds (Fig. 6). Cormorants
are opportunistic foragers, feeding primarily on benthic fish but also include
pelagic fish in their diet (Gremillet et al. 1998). They are diving hunters and
usually prefer small fish, either small species or young individuals of larger
species. Great cormorants forage up to > 20 km distance from their breeding
colony (Paillisson et al. 2004, Engström 2001).
Figure 6. Cormorant nesting on trees (A) and on the surface (B)
Cormorants are one of few seabirds with increasing numbers in Europe. Great
cormorants 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 recolonize the south of Sweden (Kalmarsund) in 1948. The
archipelago of Stockholm was recolonized in 1994. Their abundance in the
archipelago increased to 5759 breeding pairs in 21 colonies by 2007, whereafter
the population size seemed to have stabilized at about 5200 breeding pairs (Fig. 7).
(Staav 2008, 2010). The colonies in our study area are active between April and
August and span between 4 and 776 pairs (2009). During fall, most birds migrate
and overwinter in the Mediterranean and the Black Sea.
Cormorants are disliked in Sweden, as in other parts of Europe. They are
blamed by fishermen for reduced catches and by the public for damaging the
environment. However, their presence has a positive effect on threatened birds,
like sea eagles (Haliaeetus albicilla) and guillemots (Cepphus grylle), by
providing prey and creating favored nesting habitats. Despite the controversial
public discussion and the increasing cormorant density in Europe, not much
30
Number of cormorant nests
scientific research has been done on the impact of cormorant colonies on
ecosystems.
6000
5000
4000
3000
2000
1000
0
1994 1996 1998 2000 2002 2004 2006 2008 2010
Year
Figure 7. Development of cormorant population in Stockholm archipelago (Staav 2008, 2010).
Plants and invertebrates
Paper I and II focus on terrestrial plants and arthropods, paper III on aquatic algae
and invertebrates and paper IV on both terrestrial and aquatic plants and invertebrates. Chironomids, emerging insects with aquatic larvae were subject of all
studies. Paper I studied all abundant arthropod groups including the major trophic
groups: herbivores, detritivores, scavengers and predators. Paper II focused on
beetles (Coleoptera), true bugs (Heteroptera), spiders (Aranaea) and non-biting
midges (Chironomidae, Diptera). Paper III deals with Fucus vesiculosus, epiphytic
algae, and the most abundant grazers associated with Fucus, the mollusc
Theodoxus fluviatilis, the crustaceans Jaera albifrons, Gammarus spp. and Idotea
spp., and chironomids.
Lythrum salicaria – Galerucella – system (paper IV)
Purple loosestrife, Lythrum salicaria L. (Lythraceae) is an abundant perennial herb
on the shore-line in most areas of the northern Baltic Sea. The beetles Galerucella
calmariensis L. and G. pusilla L. (Coleoptera: Chrysomelidae) are monophagous
herbivores of L. salicaria (Hambäck et al. 2000).
31
Sampling and sample preparation
Soil
Per island, three soil samples were taken spread over the islands. Sampling was
carried out with a soil core (ø 3cm) at 0-10 cm depth. Samples were divided into
two layers 0-5 cm and 5-10cm depth. Samples were cooled directly after sampling
until sieving in the evening. All large organic and inorganic material was removed
from the soil samples by sieving through a 2 mm mesh sieve. Sieved samples were
frozen until further preparation.
For pH analysis 1 ml soil was dissolved in 5 ml water and pH was measured under
stirring (Swedish version of the international standard ISO 10 390:1995).
For phosphate analysis, samples with dominantly organic material were milled in a
cychlotech mill to 0.5 mm. Sandy samples were homogenized in a machine mortar
for maximum 3 minutes. Inorganic phosphorous in the milled or homogenized
samples was determined following extraction with 2% citric acid (1:5 soil to
extract solution) (Linderholm 2007). For ammonium and nitrate analysis, soils
were extracted with 2M KCl (100 g soil and 250 ml liquid) for 2 hours for sandy
soils and over night for clayey soils. Soils were filtered and analyzed on a flow
injection analyzed (Foss, Sweden), following the application notes AN 50/84
(Tecator, 1984) and ASN 50-01/92 (Tecator, 1992).
Vegetation (paper I and II)
Vegetation cover, rock cover, aboveground plan biomass, mean plant species
richness per m2, and evenness were estimated along 1 or 2 transects across the
islands in July 2007. Total plant species richness was estimated during May and
September 2007–2009 by inventories of all plants on islands.
Terrestrial arthropods
Arthropods were sampled with suction sampling, sweep-netting, pitfall trapping,
and hand collection during 2007–2009, for estimating density (paper I and II) and
species richness (paper II), and to carry out stable isotope analysis (paper I), and
carbon (C-), nitrogen (N-), and phosphorus (P-) analysis (paper IV) (Tab. 1).
Suction samples were sorted to order, families or species (Coleoptera,
Heteroptera). Spiders and coleopterans from pitfall traps and chironomids were
sorted to species. All taxa were grouped in trophic groups based on information
from the literature (Jacobs 1998) and from experienced taxonomists (H.-E.
Wanntorp, C.-C. Coulianos and Y. Brodin).
Aquatic algae and invertebrates (paper III and IV)
Fucus and its associated epiphytic algae and invertebrates were collected within
near shoreline. We randomly collected 6 Fucus fronds per island, 3 fronds per
sample site. T. fluviatilis, J. albifrons, Gammarus spp., Idotea spp., and
Chironomidae were counted and used for further analysis. To calculate the ratio of
epiphytic algae to Fucus in each sample, one branch of the Fucus frond was
cleaned from all epiphytic algae by scraping.
32
Stable isotope analysis (paper I and III)
Stable isotope analysis has become a popular tool for ecologists to elucidate the
structure of food webs, to calculate the importance of marine 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). The elements C, N, S, H and O (I focused in my thesis
on C and N) all have more than one isotope and the isotopic composition of
natural material can be measured with mass spectrometry. The isotopic
composition is expressed as δ values (‰, parts per thousand differences from a
standard):
δX = [(Rsample/Rstandard)-1] * 1000,
where X is the heavier isotope of the element (13C or 15N) and R is the isotopic
ratio (13C/12C or 15N/14N) (Peterson and Frey 1987). The δ values measures the
amount of heavy (13C and 15N) and light (12C and 14N) isotopes in a sample.
Increases in δ indicate an increase in the amount of the heavy isotope. Standard
references are for carbon international limestone standard Vienna PeeDee
Belemnite (VPDB) (δ13C) and for nitrogen atmospheric N (δ15N). Samples
enriched in the heavy isotope have a positive δ value whereas samples depleted in
heavy isotopes relative to the standard have a negative δ value.
The logic behind stable isotope analysis is that consumers typically reflect, with
some predictable changes (fractionation), the isotopic com-position of their
resources. In general, carbon isotope ratios tend to have much lower fractionation
rates than nitrogen isotope ratios (McCutchan and others 2003, Vanderklift and
Ponsard 2003). Carbon isotope ratios are clearly separated between marine and
terrestrial plants, marine primary producers are more enriched (higher (=less
negative) δ13C values) in the heavy 13C than terrestrial primary producers (lower
(=more negative) δ13C values) (Fig. 8). Thus, consumers feeding on marine algae
can be distinguished from consumers feeding on terrestrial plants by their higher
δ13C signature. Nitrogen isotopes are also slightly enriched in ocean surface
waters, but generally nitrogen isotopic ratios are more variable than carbon
isotopic ratios. Consumers are typical enriched in 15N relative to their diet
(McCutchan et al. 2003, Vanderklift and Ponsard 2003) (Fig. 8). This 15N
enrichment is mainly a result of differential protein synthesis and excretion of the
lighter isotope (Ponsard and Averbuch 1999). Thus, the tissues of marine
consumer on a high tropic level, such as fish-eating seabirds, have high 15N values
(Barrett et al. 2005) (Fig. 8). This 15N enrichment is further enhanced in seabird
guano through the fast mineralization of uric acid to ammonium (NH4+), a
chemical reaction that selectively removes 14N from guano (Mizutani et al. 1986,
Wainright et al. 1998). Soils and plants from seabird affected areas, and
consumers feeding on seabird tissue or on from seabirds fertilized plants, are
therefore enriched in 15N (Anderson and Polis 1999, Wainright et al. 1998, Barrett
et al. 2005). Thus, stable isotope values of nitrogen can be used to trace the fate of
avian nitrogen on and around islands. In my thesis I combined δ13C and δ15N
33
signatures to trace the fate of avian N and to identify trophic pathways on and
around cormorant islands.
For stable isotope analysis, animals were freeze-dried, vascular plants and algae
were oven-dried at 50°C for up to two weeks prior to analysis and sieved soils
were air dried and finely ground. Plant and animal specimens were analyzed
individually, but pooled samples were occasionally used for arthropod taxa with
individual dry weights less than 0.7 mg. When possible, only legs and heads were
used to avoid including gut contents. Stable isotope ratios for C and N of plant and
animals samples were measured with an Isotope Ratio Mass Spectrometer type
Europa integra. Stable isotope ratios of soils were analyzed on a ANCA-SL
(Sercon United Kingdom) coupled to a Sercon 20-20 IRMS.
Figure 8. Isotopic signature (δ13C and δ15N) of terrestrial and brackish primary producers and
consumers.
In paper I a single isotope (δ13C), two-source diet mixing model (IsoSource
Version 1.3.1; Phillips and Gregg 2001) was used to estimate the relative
proportion of marine and terrestrial carbon in detritivores and predators.
In paper III a dual isotope (δ13C, δ15N), two-source diet-mixing model
(Bayesian-mixing model) was used to estimated the relative proportion of Fucus
and epiphytic algae in the diet of five aquatic invertebrates with the software
MixSIR (Moore and Semmens 2008).
Before applying the diet mixing models in paper III, we standardized the lipid
content in the samples (both sources and consumers) with a mathematical
normalisation technique (Post et al. 2007). Diet mixing models in paper III were
analysed with both untreated δ13C ratios and lipid-normalized δ13C ratios because
it remains unclear if this normalization is necessary (Post et al. 2007). In paper I
34
we did not correct for the variation in lipid content among organisms or tissue
types because of the lack of reliable normalization techniques for terrestrial
organism (Post et al. 2007), the time-consuming alternative lipid extraction
method and the possibility of lipid extraction causing fractionation in δ15N
(Pinnegar and Polunin 1999; Sotiropoulos and others 2004).
In paper I we assumed a tropic shift of 0.4‰ for C (McCutchan et al. 2003). In
paper III we calculated estimates of the carbon and nitrogen fractionation factors
for each consumer by using the equations in Caut et al. (2009).
Fertilization experiment (paper IV)
For the fertilization experiments we used 225 potted plants, split into 9 treatments
(= 25 plants per treatment). Each treatment was watered with a certain level of N
(H4N2O3) and P (Na2HPO4*2H20) input. Newly hatched Galerucella larvae were
placed on the plant (15 per plant). About 4-5 weeks later Galerucella pupae were
collected from the pots.
CNP-analysis (paper II, III and IV)
Phosphorus content (%P, dry mass basis) was assayed using persulphate digestion
and ascorbate-molybdate colorimetry (Clesceri et al. 1998). Nitrogen and carbon
content (% N, % C, dry mass basis) was assayed by using Isotope Ratio Mass
Spectrometer type Europa integra or an elemental analyzer. In this analysis,
samples were oxidized and reduced to N2 and CO2, respectively, which were
measured with a thermal conductivity detector and IR-detection.
Statistics
Terrestrial island ecosystem (paper I and II)
We compared stable isotope signatures (δ13C and δ15N) of soil, terrestrial plants
and arthropods, plant and soil nitrogen and phosphorus content, soil pH and
moisture, vegetation cover, plant aboveground biomass, arthropod abundance. and
plant and arthropod species richness between three island categories (active and
abandoned cormorant islands and reference islands) in the free software R (version
2.10.0) using a one-way ANOVA, and Tukey HSD post-hoc tests, and also
performed regressions with mean nest density as explanatory variable.
Furthermore, we compared arthropod community compositions and species
composition of plants, coleopterans, heteropterans, cursorial spiders and
chironomids with np-MANOVA based on Bray-Curtis dissimilarities, using the
adonis function of the package vegan for R (version 2.10.0, Oksanen 2009). We
used 2-dimensional nonmetric multidimensional scaling (NMDS) plots to illustrate
35
the ordination of the islands. We identified indicator species for the three island
categories with the help of indicator species analysis in PC-ORD (version5,
McCune et al. 2002).
Finally, we used structural equation modeling (SEM, sem package in R 2.10.0,
Fox 2006) to separate the direct effect of mean nest density and the indirect effects
via changes in the vegetation on island arthropods (Wright 1934, Mitchell 1992).
Near shore brackish water ecosystem (paper III)
To investigate if algae and associated invertebrates near cormorant colonies
incorporate ornithogenic N in their tissue, we compared stable isotope ratios (δ13C
and δ15N) between the three groups of cormorant islands and the reference islands
with linear mixed effects models. Linear mixed effects models were also used to
test for differences in (a) the epiphytic algae to Fucus ratio, (b) nitrogen and
phosphorus content of algae and invertebrate, (c) abundance and (d) biomass of the
five invertebrate groups between reference islands and the three cormorant island
categories.
Homeostasis (paper IV)
We compared N:C, P:C, and N:P among herbivorous, detritivorous, and predatory
arthropods with linear mixed effects models. Similarly, we compared N:C, P:C,
and N:P of algae and brackish invertebrates between the three groups of cormorant
islands and the reference islands with linear mixed effects models. To test for strict
homeostasis we conducted regression analysis for N:C, P:C, and N:P for each
arthropod groups using plants as resource for terrestrial herbivores, detritivores,
and insect predators, algae (Fucus and epiphytic algae) as resource for aquatic
consumers and chironomids as resource for spider.
36
Results and Discussion
Stable isotope analysis – hypothetical food web (paper I and III)
Coccinelidae
10.4
Herbivores
11.9 (8.9-12.5)
Carabidae
9.7
Formicidae
11.9
Detritivores
Collembola 12.6
Isopoda 16.2
Nabidae
13.2
Fungivores
?
Chilopoda
16.8
Staphylinidae
15.9
Scavengers
Saprophagous
coleoptera
Brachycera 19.9
Lycosidae
11.4
Chironomidae
8.8 (adults)
11.5: (larvae)
Web
spiders
8.1
Saldidae
12.7
Aquatic invertebrates
Gammarus 8.8
Jaera 7.2
Idotea 8.1
Theodoxus 7.4
Plants
12.3
Soil food web
?
Fungi
?
Soil
12.3
Food
scrap
Cormorant
bodies
Epiphytic
algae
11.3
Fucus
11.7
Guano
Brackish
Terrestrial
Low δ13C
High δ13C
Ornithogenic N (enriched δ15N) pathway
Ornithogenic N (enriched δ15N) and marine C (enriched δ13C)
Figure 9. Simplified arthropod food web on active cormorant islands with high nest density.
Numbers indicate the increase in δ15N (Δ δ15N ‰) signature compared to reference islands.
Dashed lines reflect the flow of ornithogenic N (= enriched δ15N signatures), dashed - double
dotted lines reflect the flow of ornithogenic N (= enriched δ15N signatures) and marine C (=
enriched δ13C signatures). Thick lines indicate main flows.
Based on the stable isotope analysis and diet mixing models we constructed a
simplified food web for active cormorant islands with high nest density (Fig. 9).
Most importantly, these analyses strongly indicated (1) that especially spiders feed
largely on chironomids, (2) that ornithogenic N enters the terrestrial food web via
several pathways and travels through the whole arthropod food web, and (3) that
brackish algae and associated invertebrates incorporate ornithogenic N in their
body near active cormorant islands with high nest density. In more detail, the δ13C
signature clearly separated terrestrial plants and their primary consumers
(herbivores) and secondary consumers (coccinelids) from marine epiphytic algae
and their primary consumers (Chironomidae) and secondary consumers (webbuilding spiders) (Fig. 10). All other terrestrial consumers seemed to mix their diet
and include both terrestrial and marine sources, directly like detritivores and
37
scavengers (isopods, collembolans, brachycerid dipterans, and saprophagous
coleopterans) or indirectly by preying on these consumers (e.g. nabids, formicids,
chilopods, carabids, staphylinids). The enriched δ15N signatures (Fig. 10) showed
that all investigated plants and arthropods on active seabird islands contained some
ornithogenic nitrogen. However, chironomids and web spiders incorporated, like
brackish algae and their associated invertebrates, a significant amount of
ornithogenic N in their tissue only on/nearby cormorant islands with high nest
density (Figs. 10 and 11). On abandoned cormorant islands plants, herbivores,
detritivores, and some insect predators showed increased δ15N, whereas brackish
algae, chironomids, and spiders did not. This indicates that predators without
increased δ15N signature (spiders and saldids) fed mainly on chironomids, whereas
predators with increased δ15N fed at least partly on terrestrial prey. The diet mixing
model suggested that the diet of some of the arthropod groups differed between the
island categories. Collembolans, brachycerid dipterans, staphylinids, and saldids
seemed to include more marine carbon in their diet on active cormorant islands
than on reference islands, whereas web spiders, lycosids, and carabids proportional
seemed to include less marine carbon in their diet. Web spiders, lycosids and
nabids included the highest percentage of marine carbon in their diet on abandoned
cormorant islands.
38
Terrestrial carbon source
30
Marine carbon source
Terrestrial plants
Epiphytic algae
25
Reference island
Abandoned cormorant island
Active cormorant island
Low nest density
High nest density
20
15
10
5
0
δ15N (‰)
30
Herbivores
Collembola
Brachycera
SaproSa
phages
Coleoptera
Coccinelidae
Carabidae
Chilopoda
Staphylinidae
25
20
Isopoda
Chironomidae
Formicidae
Nabidae
Web spiders
Lycosidae
Saldidae
15
10
5
0
30
25
S
C
S
20
F
15
0
N
-30
-25
-20
-15 -30
-25
-20
-15
-30
-25
L
F F
S
C
S
W
10
5
L
N
S
F
S
N
N
S
-20
-15 -30
S
-25
-20
-15 -30
-25
W L
L W
-20
W
-15
δ13C (‰)
Figure 10. Bi-plot of δ15N and δ13C for brackish algae, terrestrial plants, and arthropods on and around islands without a cormorant colony
(= reference islands), with an abandoned cormorant colony and with an active cormorant colony (means ± SE). For some groups a subdivision of active cormorant islands into islands with a low and high nest density improved the ANOVA model.
20
C
E
15
δ13 N
J
10
T
G
I
F
T
C E J
G
I
T
J
C
E
G
T I
J
I
C E
G
5
0
-21
Reference islands
Cormorant islands
Abandoned
Active with low nest density
Active with high nest density
F
F
F
-14
-7
F
E
C
T
G
I
J
Fucus vesiculosus
Epiphytic algae
Chironomidae
Theodoxus fluviatilis
Gammarus spp.
Idotea spp.
Jaera albifrons
δ13 C
Figure 11. Bi-plot of δ15N and δ13C for brackish algae and invertebrates nearby islands without a
cormorant colony (= reference islands), with an abandoned cormorant colony and with an active
cormorant colony with low and high nest density (means).
Effects of nesting cormorant on island ecosystem
We found that cormorant nesting colonies affected soil, terrestrial vegetation and
arthropods, brackish algae and grazer (Figs. 12 and 13)
Effect of nesting cormorants on soil chemistry
Soil nitrogen content (NH4+ and NO3-) was highest on active cormorant islands and
about equal on reference and abandoned cormorant islands (F = 31.7, p < 0.001, r2
= 87.2 and F = 19.1, p = 0.001, r2 = 80.1). Soil P content was lowest on reference
islands and about equal on active and abandoned cormorant islands (F = 42.1, p <
0.001, r2 = 90.1). Soil pH and soil moisture did not differ between the three island
categories.
40
Figure 12. Effects of active nesting cormorant colonies on terrestrial and near-shore ecosystems.
Numbers indicate x-fold change. ↑ increase and ↓ decrease. A: Abundance, S: Species richness,
B: Biomass, N: percentage nitrogen content, P: percentage phosphorus content, Fu:EP:
Epiphytic algae: Fucus ratio Shown are only significant effects (p < 0.100).
Figure 13. Effects of abandoned nesting cormorant colonies on terrestrial and near-shore
ecosystems. Numbers indicate x-fold change. ↑ increase and ↓ decrease. A: Abundance, S:
Species richness, B: Biomass, N: percentage nitrogen content, P: percentage phosphorus content,
VC: Vegetation cover, E: Evenness. Shown are only significant effects (p < 0.010).
41
Effect of nesting cormorants on island vegetation (paper I, II and IV)
According to our assumption, cormorant nesting colonies strongly affected island
vegetation. The total plant species richness, the mean species richness/m2
(excluding grasses), and the vegetation cover were all lower on active than on
reference islands, whereas the plant N and P contents were higher on active
cormorant islands (Figs. 12 and 14). Abandoned cormorant islands differed neither
in vegetation cover nor in species richness from reference islands, but their
evenness was lower than on active and reference islands, whereas the plant
aboveground biomass tended to be higher on abandoned islands than on reference
islands (Figs. 13 and 14). Furthermore, vegetation cover, the total plant species
richness, the mean plant species richness/m2, and the plant nitrogen content
decreased with nest density. In contrast, plant biomass was negatively correlated
with nest density solely when including only cormorant islands in the analysis.
Active cormorant islands differ from reference islands not only in plant species
richness but also in species composition (Fig. 16). Active cormorant islands were
characterised by a few dominant nitrogen tolerant species like Galeopsis speciosa,
Urtica dioica, Tripleurospermum martimum, and Phalaris arundinacea. Common
on all active cormorant islands were Spergula arvensis and Rumex crispus,
whereas Orchidaceae and Ranunculaceae were absent.
The displayed responses of island vegetation to nesting cormorants were fairly
similar to results from fertilization experiments with decreased plant species
richness and changed plant species composition towards a few nutrient tolerant
species and increased plant nutrient content (e.g., Siemann 1998, Anderson and
Polis 1999, Haddad et al. 2000). But in contrast to fertilization experiments, on
cormorant islands primary production was not increased and vegetation cover was
decreased, due to nutrient toxication (Ellis 2005, Ellis et al. 2006).
42
b
RF
AB
CO
RF
AB
CO
1.4
b
AB
CO
RF
AB
CO
0.3
0.4
0.5
0.6
G) F = 25.7 p < 0.001
0.2
a
a
Plant phosphorus content
5.0
4.0
a
b
3.0
a
RF
CO
F) F = 24.1 p < 0.001
F = 2.8 p = 0.091
a
AB
ab
0.2
0.7
0
RF
CO
Plant nitrogen content
0.5 1.0 1.5 2.0 2.5 3.0
Aboveground biomass
(log-transformed)
E)
AB
2.0
RF
a
1.0
0.9
0.8
Evenness
b
a
a
D) F = 11.9 p < 0.001
0.6
C) F = 5.5 p = 0.015
5
4
ab
3
a
2
40
b
Mean plant species
richness/m2
60
50
ab
30
Total plant species
richness
a
Vegetation cover
(sqrt-transformed)
B) F = 3.9 p = 0.041
F = 4.8 p = 0.024
1
A)
RF
AB
CO
Figure 14. Responses of island vegetation to cormorant nesting colonies. In the calculation of
(B) and (C), grasses were excluded. Shown are median values of the response variable with
upper box showing 75th percentile, lower box showing 25th percentile and whiskers showing
values within the range of 1.5 interquartile distances. F and p were derived from one-way
ANOVA, with significant differences in bold. Different letters indicate significant differences (p
< 0.05).
Effect of nesting cormorants on island arthropods (paper I and II)
The np-MANOVA showed that the arthropod community composition differed
between island categories (total df = 17, Pseudo-F = 4.2, p = 0.001, r² = 34.6) (Fig.
15). Some but not all investigated arthropod groups responded to cormorant
colonies with changes in abundance, species richness and/or species composition.
Figure 15. 2-dimensional NMDS
of the arthropod community.
43
Density response (paper I and II)
Among the major trophic groups, collected by suction sampling (herbivores,
detritivores, scavengers, fungivores, omnivores, and predators), cormorant colonies only affected the total density of scavengers and predators per unit vegetated
area. Scavenger densities were 9 times higher on active cormorant islands than on
reference islands and were about equal when comparing abandoned and reference
islands. Predator densities were 3 times higher on abandoned than on reference
islands but did not differ between reference and active cormorant islands. The
positive density responses of scavengers and predators were also reflected in their
mass response (= total wet weight per unit area). Moreover, herbivores, in contrast
to their density response, had 3 times higher mass on active cormorant islands than
on reference islands.
In suction samples, the density of 11 of 18 arthropod groups differed between
island categories (Figs. 12 and 13, Tab. 3). Six groups had higher (herbivores:
lepidopteran larvae and aphids, scavengers: brachycerid dipterans and
saprophagous coleopterans, predators: parasitic hymenopterans and aphidophages)
and two had lower (collembolans and lycosids) densities on active cormorant than
on reference islands. On abandoned cormorant islands, two groups (lepidopteran
larvae and web spiders) had higher densities than on reference islands and one
group (herbivorous coleopterans) had higher density than on active cormorant
islands. Chironomids responded to active cormorant colonies with increased
densities only if the colonies had a high nest density.
For pitfall trap samples, neither the total abundance of coleopterans nor the
total abundance of spiders responded to cormorant nesting colonies. The division
of coleopterans in major feeding groups (herbivores, fungivores, algaevores,
saprophages and predators) showed that herbivores tended to have lower
abundance on active cormorant islands than on reference islands, whereas
fungivores and saprophages were more abundant on active than on reference
islands (Fig. 12, Tab. 3). Chironomids showed no difference in abundance
between the island categories but increased with nest density.
Response in species richness (paper II)
Of the five investigated groups (coleopterans and heteropterans collected by
suction sampling, coleopterans and cursorial spiders caught in pitfall traps, and
chironomids caught with sweep netting) showed no significant difference in the
observed species richness among island categories; but spiders tended to have
lower observed species richness on active cormorant islands than on reference
islands (Fig. 12, Tab. 3) Heteropterans tented to have higher observed species
richness on abandoned islands than on reference islands (Fig. 13). The estimated
species richness of coleopterans in pitfall trap samples was higher whereas the
estimated species richness of spiders was lower on active cormorant islands than
on reference islands. For suction samples, the subdivision into feeding groups
showed that the highest species richness of herbivorous heteropterans and
fungivores coleopterans was found on abandoned islands (Fig. 13, Tab. 3). For
pitfall trap samples, the subdivision showed that fungivorous and saprophagous
44
coleopterans had higher numbers of species on active cormorant islands than on
reference islands (Fig. 12, Tab. 3). The species richness of herbivorous
coleopterans differed not between the islands categories but decreased, as the
species richness of spiders, with increasing nest density.
Table 3. One-way ANOVA of mean abundance (log-transformed), observed and estimated
species richness of arthropods on active (AO) and abandoned (AB) cormorant islands with
reference (RF) islands.
Taxa
df, Error df
F
p
adj. r2
RF AB AO
2, 16
4.7
0.024
29.4
X=X>Y
0.000
67.8
DVac
Herbivores
Aphidoidae
Abundance
Lepidoptera larvae
Abundance
2, 16
20.0
Cicadina
Abundance
2, 16
n.s.
Coleoptera
Abundance
Ob. sp. rich.
2, 16
6.2
n.s
0.010
36.7
Heteroptera
Abundance
Ob. sp. rich.
2, 16
n.s.
4.8
n.s.
0.022
29.9
Collembola
Abundance
2, 16
7.1
0.006
40.5
Isopoda
Abundance
2, 16
n.s.
Coleoptera
Abundance
Ob. sp. rich.
2, 16
2.8
6.7
0.090
0.008
16.7
38.7
X=X=X
X < Y =XY
Brachycera (Diptera)
Abundance
2, 16
19.5
0.000
67.3
X=X<Y
Coleoptera
Abundance
Ob. sp. rich.
2, 16
10.7
4.3
0.001
0.032
51.8
26.9
X=X<Y
X = XY < Y
Web spiders
Abundance
2, 16
4.9
0.021
30.5
X < Y = XY
Lycosidae
Abundance
2, 16
11.2
0.001
53.1
Other spiders
Abundance
2, 16
n.s.
Aphidophaga
Abundance
2, 16
9.2
0.002
47.6
X=X<Y
Parasitic Hymenoptera
Abundance
2, 16
5.3
0.017
32.5
X = XY < Y
Coleoptera
Abundance
Ob. sp. rich.
2, 16
n.s.
n.s.
X=X=X
X=X=X
Carabidae
Abundance
2, 16
n.s.
X=X=X
Staphilinidae
Abundance
2, 16
n.s.
X=X=X
Heteroptera
Abundance
Ob. sp. rich.
2, 16
n.s.
n.s.
X=X=X
X=X=X
Chilopoda
Abundance
2, 16
n.s.
Chironomidae *
Abundance
3, 15
3.2
Abundance
Ob. sp. rich.
Est. sp. rich.
2, 11
n.s.
n.s.
4.2
Herbivorous coleoptera
Abundance
Ob. sp. rich.
2, 11
Fungivorous coleoptera
Abundance
Ob. sp. rich.
2, 11
X >Y = Y
X = X =X
XY= X > Y
X<Y>X
Detritivores/Fungivores
X = XY > Y
X=X=X
Scavengers
Predators
X=X>Y
X=X=X
X=X=X
0.052
27.3
X=X=X
0.044
32.9
X=X=X
X=X=X
X = XY < Y
3.0
n.s.
0.093
23.3
X=X=X
X=X=X
9.9
6.9
0.003
0.011
57.9
47.7
X = XY < Y
X = XY < Y
Pitfall traps
Coleoptera
45
Algaevorous coleoptera
Abundance
Ob. sp. rich.
2, 11
n.s.
n.s.
Saprophagous coleoptera
Abundance
Ob. sp. rich.
2, 11
5.1
7.4
Predatory coleoptera
Abundance*
Ob. sp. rich.
2, 11
n.s.
n.s.
Araneae
Abundance
Ob. sp. rich.
Est. sp. rich.
2, 11
n.s.
3.4
4.4
Abundance
Ob. sp. rich.
Est. sp. rich.
2, 9
n.s.
n.s.
n.s.
X=X=X
X=X=X
0.027
0.009
38.7
49.5
X = XY < Y
X=X<Y
X=X=X
X=X=X
0.072
0.039
26.8
34.6
X=X=X
X=X=X
X = XY > Y
Sweep-netting
Chironomidae
X=X=X
X=X=X
X=X=X
* active cormorant islands subdivided into islands with low and high nest density
Species composition (paper II)
The species composition of coleopterans and spiders, but not of heteropterans and
chironomids, differed between the island categories (Fig. 16). Active cormorant
islands were characterised by the saprophagous families Nitidulidae and Silphidae,
the mainly aphidophagous family Coccinelidae and fungivorous species.
Reference islands were characterised by the spider family Tetragnathidae and the
lycosids Alopecosa pulverulenta and Pardosa lugubris.
46
Figure 16. 2-dimensional NMDS of plants and arthropod species.
47
Direct versus indirect effects of nesting cormorants (paper II)
Island consumers might have responded directly to cormorants by utilizing their
dead and living bodies, food scrap, and eggshells (Polis and Hurd 1995, SanchezPinero and Polis 2000) or indirectly by responding to the described changes in the
vegetation (Barrett et al. 2005) or to the changes in soil chemistry, structure and
subsequent changes in microfauna and -flora (Fukami et al. 2006). Thereby
changes at the level of primary consumer can cascade up the food web and affect
consumers on higher trophic levels (Hunter and Price 1992, Polis and Hurd 1995,
Barrett et al. 2005). In order to separate direct and indirect effects of nesting
cormorants I used structural equation analysis, including mean nest density and
three vegetation variables (vegetation cover, plant biomass, and plant species
richness). Unfortunately, I was not able to include further important factors in the
analysis like plant and soil N and P content, plant species composition, fungal
biomass, and amount of carcass.
Plant N and P content are assumed to limit herbivorous and detritivorous
insects (White 1993, Cross et al. 2003) and thus I expected to find high herbivore
and detritivores densities on active cormorant islands. This expectation was only
partly met by my results. I found only aphids and lepidopteran larvae to have
increased densities on active cormorant islands, indicating that other vegetation
variables also play an important role in determining consumer abundance.
Accordingly, structural equation analysis indicated that the abundance of
lepidopteran larvae, auchenorrhynchans, herbivorous, fungivorous and predatory
coleopterans and web spiders increased with plant biomass (Figs. 17 and 18)
consistent with results from fertilization experiments (Siemann 1988, Haddad et al.
2000). Furthermore, plant biomass mainly had a positive effect on consumer
species richness supporting the hypothesis of a positive relationship between
consumer species richness and plant productivity (Waide et al. 1999, Mittelbach et
al. 2001). Also vegetation cover had strong effects on the abundance and species
richness of several beetle feeding groups, showing that vegetation cover, may
determine the assemblage of epigeal coleopterans (Frank and Reichhart 2004, Eyre
and Luff 2005). In contrast to previous studies, effects of increased cover on beetle
abundance and species richness were generally negative, except for herbivorous
beetles, perhaps due to factors correlated with vegetation cover but not included in
the models (e.g., soil chemistry). One surprising results from the structural
equation analysis was that plant species richness had, despite the positive effect on
the species richness of predatory coleopterans, no or negative effect on consumer
species richness. This contrasts with the habitat heterogeneity hypothesis
(MacArthur and MacArthur1961) and with previous empirical studies (Siemann et
al. 1998, Haddad et al. 2000). However, the apparent effect of plant species
richness on predatory coleopteran and spider species richness and web spider
abundance was more expected and supported the view of strong importance of
structural and species diversity of the vegetation for arthropod diversity (Dennis et
al. 1998, Perner et al. 2003, Garcia et al. 2009). Finally, the structural equation
analysis indicated that cormorants also directly affected several groups; positively
(saprophagous beetles, predatory coleopterans and web spiders) and negatively
48
(algaevorous coleopteran). Interestingly, the model showed a postive correlation of
brachycerid flies and parasitic hymen-opterans indicating a bottom-up control.
One weakness in my study is that I did not include the soil food web, making it
difficult to understand the response of some consumer groups. For example, it was
very surprising to find the highest density of fungivorous beetles on active
cormorant islands, because former studies show that high nitrogen loads due to
nesting seabirds negatively affect soil fungal biomass (Wright et al. 2010).
Similarly, the negative effect of cormorants on the lycosid density and on species
richness of cursorial spiders was suprising because the increased abundances of
scavengers and bird parasites in other seabird island systems were shown to
increase spider densities (Polis and Hurd 1995). One possible explanation might be
changes in soil chemisty and surface structure (Bultman and Uetz 1984, Hurd and
Fagan 1992).
A) Abundance of arthropods in the herb layer (except coleopterans and
heteropterans) (Dvac)
X² = 27.1, df = 33, P = 0.76
Path Coefficient
<0.4
0.4-0.5
0.5-0.6
0.6-0.7
0.7-1.0
>1.1
Lepidopteran
larvae
Vegetation
cover
-0.81***
Mean nest
density
0.56**
0.52*
Plant biomass
-0.47**
0.58***
-0.51*
Plant species
richness
0.46*
Auchchenorrhyncha
Brachycera
0.80***
Parasitica
0.41*
Aphidophaga
0.46*
Web spiders
A) Abundance of arthropods in the herb layer (except coleopterans and
heteropterans) (Dvac)
X² = 27.1, df = 33, P = 0.76
Path Coefficient
<0.4
0.4-0.5
0.5-0.6
0.6-0.7
0.7-1.0
>1.1
Lepidopteran
larvae
Vegetation
cover
-0.81***
Mean nest
density
0.56**
0.52*
Plant biomass
-0.47**
0.58***
-0.51*
Plant species
richness
0.46*
Auchchenorrhyncha
Brachycera
0.80***
Parasitica
0.41*
0.46*
Aphidophaga
Web spiders
49
C) Abundance of coleopterans and heteropterans (D-vac)
Χ² = 35.0, df = 31, p = 0.29
Path Coefficient
< 0.4
0.4–0.5
0.5–0.6
0.6–0.7
0.7–1.0
> 1.1
Vegetation
cover
–0.81***
Mean nest
density
Herbivorous
coleoptera
0.60***
Plant biomass
0.52***
–0.51***
0.39*
–0.51*
–0.41**
Plant species
richness
Fungivorous
coleoptera
0.74***
Saprophagous
coleoptera
0.63**
0.41*
Predatory
coleoptera
Predatory
heteroptera
D) Species richness of coleopterans and heteropterans (D-vac )
Path Coefficient
< 0.4
0.4–0.5
0.5–0.6
0.6–0.7
0.7–1.0
> 1.1
Χ² = 19.3, df = 26, P = 0.830
0.56**
Vegetation
cover
0.58***
–0.83***
Mean nest
density
0.31*
–0.51*
Plant biomass
–0.56**
0.43*
Plant species
richness
0.39
0.51*
Herbivorous
coleoptera
Fungivorous
coleoptera
Predatory
coleoptera
Herbivorous
heteroptera
Predatory
heteroptera
Figure 17. Path diagram for effects of cormorant nest density on vegetation variables and
arthropods from suction sampling on 19 islands. Approximate path coefficients are indicated by
thickness of arrows. Solid lines indicate positive relationships, broken lines negative
relationships. Asterisks (*) indicate the level of significance: p < 0.05*, p < 0.01**, p <
0.001***.
50
Herbivorous
coleoptera
A) Abundance (pitfall traps)
X2 = 21.3, df = 25, p = 0.67
–0.67**
–1.11***
0.42***
–0.78***
–0.78*
Mean nest
density
Plant biomass
Algaevorous
coleoptera
0.37*
0.86***
Plant species
richness
0.70**
0.61*
–0.71**
Path Coefficient
< 0.4
0.4–0.5
0.5–0.6
0.6–0.7
0.7–1.0
> 1.1
0.49***
–0.92**
Vegetation
cover
–0.63**
Fungivorous
coleoptera
0.74***
Saprophagous
coleoptera
–0.52***
–1.3***
1.42***
Predatory
coleoptera
1.0***
Araneae
B) Species richness (pitfall traps)
Herbivorous
coleoptera
X2 = 21.5, df = 28, p = 0.80
0.47
–0.84***
Vegetation
cover
–0.78***
Mean nest
density
Path Coefficient
< 0.4
0.4–0.5
0.5–0.6
0.6–0.7
0.7–1.0
>1.1
–1.11***
–0.71***
–0.75*
–0.87***
Plant biomass
Plant species
richness
Fungivorous
coleoptera
0.36*
0.35*
Algaevorous
coleoptera
0.50*
–0.43
Saprophagous
coleoptera
1.08***
1.12***
0.41*
0.43*
Predatory
coleoptera
Araneae
Figure 18. Path diagram for effects of cormorant nest density on vegetation variables and
Coleopteran and Araneae from pitfall trapping on 13. Approximate path coefficients are
indicated by thickness of arrows. Solid lines indicate positive relationships, broken lines
negative relationships. Asterisks (*) indicate the level of significance: p < 0.05*, p < 0.01**, p <
0.001***.
51
Effects of cormorant nesting colonies on algae and aquatic invertebrates in
coastal waters (paper III)
The effects of nutrient input by nesting cormorants were not limited to the
terrestrial system, but also included adjacent aquatic systems, or more precisely the
Fucus-epiphytic algae-invertebrate complex in near shore waters (Fig. 12). These
effects were only visible around active cormorant islands with high nest density.
Accordingly, algae nearby cormorant islands had enriched δ15N signatures only
when the colony had a high nest density. This indicates that significant nutrient
runoff from cormorant islands into surrounding waters only occur if the nest
density exceeds a certain level. On islands with low nest densities, vegetation takes
up most ornithogenic N and P in plant biomass. The nutrient load on cormorant
islands with high nest densities, especially the ammonia load, which is toxic,
suppressed plant growth and caused a decreased vegetation cover. The nutrient
input to the terrestrial systems exceeded the amount that can be bound in soil and
vegetation and notable amounts of nutrients run off into the sea.
Thus, primary producers around high nest density islands responded as in
previous fertilization and mesocosm studies, with an increased epiphytic algae
load (Worm et al. 2000, Råberg and Kautsky 2008) (Fig. 19). Furthermore, the N
and P contents of algae near active cormorant islands with high nest density were,
similar to terrestrial plants, 1.6 and 1.5 higher than near reference islands (Fig. 19).
Contrary to previous studies from the Baltic Sea (Kotta et al. 2000, Worm and
Sommer 2000, Kraufvelin et al. 2006, 2007) and Lake Michigan, US
(Blumenshine et al. 1997), not all invertebrates responded with increased
abundance. Three of five invertebrate taxa (Jaera albifrons, Gammarus spp., and
Chironomidae) showed increased biomass near islands with high nest density, but
only J. albifrons increased in abundance compared to reference islands (Fig. 20).
The lacking response of Idotea spp. and T. fluviatilis may be the role of Fucus as a
habitat, providing shelter against disturbance or predation (Orav-Korra and Kotta
2004, Wikström and Kautsky 2007, Råberg and Kautsky 2007). The large Idotea
spp. may be more dependent on Fucus as a shelter than the smaller J. albifrons,
Gammarus spp., and Chironomidae and thus suffer from the relative decrease of
Fucus. Furthermore, the diet mixing model indicated that Idotea spp. did not
prefer epiphytic algae as food source as strongly as the other invertebrates and had
a relatively higher Fucus consumption. T. fluviatilis might similarly suffer from
decreased shelter but also from the increased filamentous algae load that competes
with microalgae, an important food source for the scraping snails (Råberg and
Kautsky 2008).
52
0.10 0.15 0.20 0.25
Fucus vesiculosus
0.06
*
0.02
%P
0.10
A)
RF
AB
COL
*
RF
COH
AB
COL
COH
Epiphytic algae
5
5
4
Fucus vesiculosus
4
B)
Epiphytic algae
0
0
1
1
2
3
3
*
2
%N
**
RF
AB
COL
COH
RF
AB
COL
COH
1.5
1.0
RF
0.5
**
0.0
Epiphytic algaeFucus ratio
C)
RF
AB
COL
AB
COL
COH
Reference Islands
Cormorant islands
Abandoned
Active with low nest density
Active with high nest density
COH
Figure 19. Nitrogen (A) and phosphorus (B) algal content and epiphytic algae:Fucus ratio (C) in
near-shore waters of four island categories. Shown are median values of the response variable
with upper box showing 75th percentile, lower box showing 25th percentile and whiskers
showing values within the range of 1.5 interquartile distances. (•) P < 0.1, * P < 0.05, ** P <
0.01, *** P < 0.001 refer to level of significances relative to reference islands.
53
Theodoxus fluviatilis
0
4
1
0
Gammarus spp.
0
0
1
16
48
**
4
9
144
Idotea spp.
2.25
Jaera albifrons
1.0
Invertebrate biomass (mg dry-weight per g algae)
16
**
(•)
36
4
48
9
100
Chironomidae
AB
RF
Reference Islands
Cormorant islands
Abandoned
Active with low nest density
Active with high nest density
AB
COL
COH
COL
COH
0
0.25
**
RF
RF
AB
COL
COH
Figure 20. Biomass (sqrt-transformed) of marine invertebrates (number of individuals per gram
dry-weight algae) collected in near shore waters of four islands. Shown are median values of the
response variable with upper box showing 75th percentile, lower box showing 25th percentile and
whiskers showing values within the range of 1.5 interquartile distances (•) P < 0.1, * P < 0.05,
** P < 0.01, *** P < 0.001 refer to level of significances relative to reference islands
My results in context of other seabird island studies
The effect of nesting seabirds on island vegetation has been intensively studied
and my results are, generally, consistent with previously studies (see metaanalysis
by Ellis et al. 2011, see metaanalysis by Mulder et al. 2011). However, not much
work has been done on the effects of nesting seabirds on island consumers and the
majority of studies have been concentrated in two regions: the Gulf of California,
Mexico and New Zealand. The intensive studies in these regions give good
insights on processes in these systems, but not about the effect of nesting seabirds
on island consumers in general. Both systems are unique; the Gulf of Mexico with
its hot-dry climate with irregular rain-pulses (El Niño Southern Oscillation) and
54
New Zealand with burrowing seabirds. Therefore, I find my study to be an
important contribution on the effects of nesting seabirds in other regions. The
majority of studies on seabird island consumers found higher consumer
abundance, survival and reproduction rates (reviewed by Kolb et al. 2011). This
indicates that seabird islands are mainly bottom-up regulated systems with
consumers being positively affected by enhanced resources from seabirds.
However, several biotic and abiotic factors, like life history traits of seabird taxa,
timing of seabird inputs, nesting density, history of seabird use of islands, climate
and seasonality, inputs of other marine subsidies, trophic cascades, and apparent
com-petition are likely to affect the magnitude or even direction of consumer
responses.
In my study systems the lack of positive numeric response might be partly
caused by the lack of food limitation of the consumers, due to high amounts of
shore drifted algae and high abundances of chironomids. These highly abundant
food sources may shift consumer population from being limited by food to being
limited by habitat. This might be the case for spiders in our systems, for examples
the high abundance of web spiders on abandoned cormorant islands might be
explained by the increased biomass and heterogeneous vegetation and thus
increased substrate for web-building (Miyashita and Takada 2007, Chan et al.
2009). Another possible explanation for lacking positive consumer response might
be top-down control. Food webs are rarely simple and linear, and the real
complexity of food webs, including competition and differential predation can
complicate the visible responses of consumers to seabirds. For example, in an
analysis of belowground community changes on seabird islands in New Zealand,
herbivorous nematodes and secondary consumers increased in contrast to primary
consumer microflora compared with non-bird islands (Fukami et al. 2006). The
most likely explanation for this observation is that the increase in secondary
consumers may have overwhelmed the bottom-up benefits the primary consumers
received from increased nutrient availability. Generally, if predator interactions are
very strong there might be no increase in abundance of lower level consumers.
In order to draw general conclusions about the effects of nesting seabirds on
island consumers further research is needed, including controlled studies on the
impact of seabird nesting density on consumer with different life history traits. To
be able to make prediction of the role of abiotic factors, like climate, more
compressive studies in different climate regions are necessary.
Compared with terrestrial systems, relatively little research has been done on
effects of seabird colonies on adjacent aquatic, especially marine, systems. My
study system differs in three major points from earlier studies. First, the Baltic Sea
has no real tides, second the water is brackish, and third the relatively small size of
colonies. Despite these differences I found, in accordance with the majority of
former studies, increased algae nutrient content, increase growth of ephemeral
algae near seabird islands and invertebrate responses. However, my study is one of
the few studies that used stable isotope analysis and thus could determine the
ornithogenic origin of the nitrogen with great certainty. Generally, relative little
consensus exists about the types and magnitudes of seabird effects on marine
55
systems because the systems in such studies vary climatically, in structure,
sampling methods used, and response variable used (reviewed by Young et al.
2011). Thus more studies on the near-shore communities of seabird islands that
use stable isotope analysis are needed to be able to draw conclusions about the
general pattern of seabird effects on near-shore communities.
Plant and consumer stoichiometry and homeostasis under nutrient
enrichment
Effects of fertilization on plant and herbivore homeostasis and herbivore
survival and body size – the Lythrum salicaria – Galerucella spp. system
(paper IV)
The outcome of the fertilization experiment supported the in ecological
stoichiometry common, simplified assumption that autotrophs (plants) are
stoichiometrically plastic while heterotrophs (animals) are strictly homeostatic
(Sterner et al. 1992, Sterner and Elser 2002). The elemental composition of
Lythrum salicaria varied strongly in accordance with the nutrient treatment (Fig.
21). Generally, plants fertilized with N and/or P had higher N:C and/or P:C ratios
than unfertilized plants. Plant N:C varied between the treatment up to 8.3 fold,
plant P:C up to 6 fold . In contrast, Galerucella spp., generally, strongly regulated
their stoichiometry, showing strong N:C and N:P homeostasis and strict P:C
homeostasis (1/HN:C≈ 0.08; 1/HN:P ≈ 0.06) (Fig. 21). However, contrary to the
general assumption that herbivores are nutrient limited (White 1993, Cross et al.
2003) and findings of previous studies that increased nutrient plant content
positively affect herbivore growth, survival and reproduction (Mattson 1080, Joern
and Behmer 1997, Frost and Elser 2002) we found no strong effects of fertilization
treatment on Galerucella survival and mean larvae dry-mass.
56
(B)
(A)
N:C (L. salicaria)
0.12
0.08
0.04
0
n
np
nP
N
Np
NP
p
P
no
Log (Galerucella N:C)
-0.6
0.16
-1
-1.4
-1.8
-1.8
-1.4
-1
-0.6
Log (L. salicaria N:C)
-0.5
Log (Galerucella P:C)
P:C (L. salicaria))
0.016
0.012
0.008
0.004
0
n
np
nP
N
Np
NP
p
P
-1
-1.5
-2
-2.5
no
-2.5
-2
-1.5
-1
-0.5
Log (L. salicaria P:C)
1.8
50
40
30
20
10
0
n
np
nP
N
Np
NP
Fertilizer
p
P
no
Log (Galerucella N:P)
N:P (L. salicaria)
60
1.4
1
0.6
0.2
0.2
0.6
1
1.4
1.8
Log (L. salicaria N:P)
Figure 21. Elemental ratios (N:C, P:C, N:P) (mean ± SE) of Lythrum salicaria under different
fertilization (A) and Regressions between Galerucella spp. and L. salicaria elemental ratios (B).
Ecological stoichiometry and homeostasis of plants and invertebrates on and
nearby heavily fertilized cormorant nesting islands (paper IV)
This study investigated the stoichiometry and homeostasis of primary producers
and invertebrates, both on and around cormorant and non-cormorant islands. I then
looked for causal relationships between stoichiometry and the level of homeostasis
of a taxonomic group, respectively, and observed numeric responses on cormorant
islands. I found in accordance to principal stoichiometric theories that
heterotrophs, generally, were in contrast to stoichiometrically plastic autotrophs,
strongly homeostatic (e.g.; Sterner and Elser 2002). All primary producers
(terrestrial plants, brackish macroalgae, and epiphytic algae) on or nearby nutrient
rich cormorant islands contained higher N:C and P:C ratios in their tissue than on
or nearby reference islands, while all herbivores, detritivores, and predators,
except spiders, kept their elemental body ratios strongly homeostatic (Fig. 22). A
potential weakness is that I tested for homeostasis mainly within families or orders
57
and not within species since I was unable to sample the same species across all
islands. Within families or orders, apparent homeostasis may not only be caused
by stoichiometric plasticity of species but also by shifts in species composition
from the dominance of nutrient poor species reference islands towards the
dominance of nutrient rich species on cormorant islands (Elser et al. 1996, Urabe
et al. 2002, DeMott and Pape 2005). However, while my focus on taxonomic
levels higher than species may reduce our ability to deduce mechanism from
pattern, effects on higher trophic levels should be similar, at least for generalist
consumers.
In accordance with previous studies (Mattson 1980, Strong et al. 1984, White
1993, Fagan et al. 2002), terrestrial herbivores and detritivores and brackish
grazers generally fed on diets containing less nutrients than themselves, while only
predators specialized on nutrient-poor preys (e.g., Coccinelidae) consumed nutriaent-poor diet, relative to their tissue chemistry. Thus, I expected herbivores and
detritivores to respond positively to increased plant nutrient content on cormorant
islands (e.g., Slansky and Feeny 1977, White 1993, Joern and Behmer 1997, Cross
et al. 2003). The numeric responses observed (paper I and III) partly supported this
assumption but also detected large variation among taxonomic groups. According
to stoichiometric theory and strong empirical support, mainly from aquatic
systems, the nutrient demand of a given taxon is determined by its nutrient content
and relative growth rate (Elser et al. 1996, Sterner and Elser 2002). Taxa (or
specific life stage) with high body N and P content and high growth rates have a
high nutrient demand to maintain growth rate and consequently secondary
productivity and thus are more sensitive to nutrient limitation than nutrient poor,
slow growing taxa (Urabe and Watanable 1992, Elser et al. 1996, Urabe et al.
2002). Hence we hypothesised that within a trophic group nutrient rich consumer
groups will be more favoured by increased nutrient availability on cormorant
islands and thus display a stronger positive response on these islands than nutrient
poor species. However, in contrast to our hypothesis the nutrient content of
herbivores and detritivores explained only numeric responses observed in one
group; lepidopteran larvae had the highest P:C among terrestrial insects and had,
as expected, higher densities on islands with high plant P content (= cormorant
islands) than on islands with low plant P content (= reference islands). Thus, our
data indicates that species traits other than nutrient content, such as e.g.,
conversion efficiency, respiration rates, host plant obligations, diet specialization,
and habitat specialization (Hall et al. 2004, Moretti and Legg 2009) may mainly
determine the success of a taxon in a certain environment.
Likewise, in contrast to our assumption, variation in homeostasis among taxa
was seemingly a poor predictor of numerical responses. Furthermore, since we
found all terrestrial herbivores and detritivores to strongly regulate their stoichiometry, increased abundances of higher consumers (e.g., Coccinelidae and parasitic
hymenopterans) were not caused by increases in prey (e.g., aphids, lepidopterans)
quality but quantities.
58
(A) Terrestrial arthropods
(B) Brackish invertebrates
-0.4
Log (Consumer N:C)
-0.6
-0.8
-1
-1.2
-1.4
-1.6
-1.8
Herbivores/
Detritivores
Predators
-1.8 -1.6 -1.4
-1.2
-1
-0.8 -0.6 -0.4
-1.8 -1.6 -1.4
Log (Resource N:C)
-1.2
-1
-0.8 -0.6 -0.4
Log (Resource N:C)
-0.5
log (Consumer P:C)
-1
-1.5
-2
-2.5
Herbivores/
Detritivores
Predators
-2.5
-2
-1.5
-1
-2.5
-0.5
Log (Resource P:C)
-2
-1.5
-1
Log (Resource P:C)
-0.5
Log (Consumer N:P)
1.6
1.4
1.2
1
0.8
0.6
0.4
Herbivores/
Detritivores
Predators
0.2
0.2 0.4
0.6 0.8
1
1.2
Log (Resource N:P)
1.4 1.6
0
0.2 0.4
0.6 0.8
1
1.2
1.4 1.6 1.8
Log (Resource N:P)
Figure 22. 3 Regressions between consumer and resource N:C, P:C and N:P for (A) terrestrial
arthropods from active, abandoned and non-cormorant and (B) brackish invertebrates nearby
active, abandoned and non-cormorant. Black lines indicate regressions with p<0.1 (plastic), grey
lines indicate regressions with p>0.1 (strictly homeostatic), drawn lines indicate herbivores and
detritivores, and dashed lines indicate predators.
59
Concluding remarks
Visiting a cormorant nesting island, it becomes pretty obvious that nesting
cormorants strongly affect the vegetation of their nesting islands. After a few years
of colonization some or most trees have died due to ammoniac poisoning. The
plant species richness and vegetation cover was decreased and plant species
composition has changed. These effects on island vegetation are especially
pronounced on islands with high nest density. Such islands cause some people to
claim that cormorants kill their nesting islands or even the whole archipelago.
Well, I found none of my study islands to be dead. The vegetation on abandoned
cormorant islands were in terms of species richness similar to non-cormorant
islands, but produced more biomass. Even on active cormorant islands with high
nest densities I found living plants and all cormorant islands harbored a variety of
arthropods. Some arthropod groups (e.g., lepidopteran larvae, herbivorous beetles)
responded to the modifications in vegetation structure or nutrient content, other
more ground living taxa (e.g., collembolans, fungivores beetles and cursorial
spiders) were seemingly affected by alterations in soil chemistry and structure,
while further groups (e.g., brachycerid flies, saprophagous beetles) responded
directly to cormorant subsidies. Consumer responses included changes in species
composition and both increases and decreases in abundance and species richness;
however, not all taxonomic or feeding groups responded to the presence of
cormorants. Differences in consumer nutrient content poorly explained numeric
response observed among taxonomic group. Similarly, no causal relationship
between the level of homeostasis and displayed numeric response could be found,
since consumers, generally, kept their stoichiometry strongly homeostatic. This
strong consumer homeostasis evidenced that bottom-up effects of cormorant
nutrients on higher trophic consumer acted not via increases in prey quality but
quantity. Thus, I found two likely bottom-up cascades, one via guano – increased
plant nutrient content – increased aphid density – increased aphidophage density
and the other via seabird carcasses and food scrap – increased brachycerid fly
density – increased parasitic hymenoptera density.
When evaluating the impact of cormorant nesting colonies on species diversity
one should distinguish between species diversity on the nesting islands and species
diversity in the whole archipelago. Even if cormorants decrease the species
richness of plants and some invertebrate groups on nesting islands, they also
change the species compositions and thus likely the beta-diversity (= species
turnover) among islands. Furthermore, active and abandoned cormorant islands
may increase the habitat heterogeneity in the archipelago by adding islands
different in plant species composition, soil chemistry, resource availability, and
portion of dead wood. Such increased habitat heterogeneity can be assumed to
increase the total species richness of archipelago.
An important factor in my thesis was, as demonstrated by stable isotope analysis,
that when studying arthropod food webs and communities on small islands in the
60
Baltic Sea one has to include the adjacent brackish ecosystem. Emerging insects
with aquatic larvae (mainly chironomids) are an important prey for major island
predators (mainly spiders) and thus pose a possibility for feed-back loops between
the brackish and terrestrial system. Such feed-back loops may be likely for active
cormorant islands with high nest densities, where δ15N analyses of brackish algae
and associated invertebrates have indicated that significant amounts of
ornithogenic nutrient run off in surrounding waters and enters the brackish food
web via algae and caused increased chironomid biomass. The high nutrient content
in the water column nearby high nest density islands caused increases in the
epiphytic algae biomass relative to Fucus biomass and thus had similar conesquences as reported in studies investigating the effects of eutrophication in the
Baltic Sea. Even if some grazers responded, like chironomids, with increased
biomass, the decrease of Fucus may lead to a decreased abundance and species
richness of larger invertebrates, or even fishes, which are dependent on Fucus as a
habitat in a long time perspective (Råberg and Kautsky 2008). However, I do not
expect seabird colonies in the Baltic Sea or other marine systems to cause serious
eutrophication problems, because they rather remove nutrient by transporting
them, as shown, to land and, furthermore, the area affected by seabird nutrient
input is restricted to the local surrounding of the colonies.
61
Further research
During my PhD study I met several interesting question which fall outside the
scope of my work but whose answers may nevertheless be crucial for
understanding the effects of nesting cormorants on island communities in
particular and the effects of increase nutrient loads on community and food web
structure, dynamic and interactions of the recipient system in general. For
example,
 When using stable isotope analysis and diet mixing models, two factors may
confound the outcome: lipid content and fractionation. The quantitative role
of these factors necessitates controlled diet experiments.
 In my study I did not include the soil food web and hence was not able to
understand responses of several ground living taxa, and how nesting
seabirds affect the interaction between below- and aboveground ecosystem.
 In my work I focused on bottom-up effects and disregarded top-down
effects. Thus, I would like to investigate the role of top-down effects in
dependence of nutrient and resource availability.
 One weakness in paper IV is that I often compared the homeostasis within
families or orders and not within species. Thus, it would be interesting to
collected the same species on all study islands and, additionally, use these
species in controlled diet experiments.
 I found that ornithogenic nutrient also entered the surrounding waters, but I
did not measure quantities and qualities. It would be interesting to
quantitatively measure the nutrient flows from the islands, the nutrient
content in the water columns nearby seabird islands and use this
information, together with data on the algal responses, to conduct ecological
network analysis in order to study changes food web functioning.
 Seabirds are worldwide declining dramatically in numbers. In order to
understand consequences from this decrease on the island, we need far more
studies on the effects of nesting seabirds on terrestrial and marine
ecosystem, in a wider range of island systems.
62
Acknowledgement
I gratefully acknowledge my supervisors P. A. Hambäck and L. Jerling for helpful
comments on this summary and, additionally, J. Hansen for help wit the Swedish
summary. I also thank L. Jerling, B. Jerling, E. Jerling, S. Jerling, H. Axemar, M.
Enskog, J. Ekholm, C. Essenberg A. Lindström, C. Palmborg and A. Sjösten for
help in the field and in the lab and H.-E. Wanntorp, C.-C. Coulianos, and Yngve
Brodin for help in identifying Coleoptera, Heteroptera, and Chironomidae.
Funding was provided by the Swedish Research Council Formas (to PAH).
63
References
Abrams PA (1995) Monotonic or unimodal diversity productivity gradients - what
does competition theory predict. Ecology 76:2019-2027
Anderson TR, Hessen DO, Elser JJ, Urabe J (2005) Metabolic stoichiometry and
the fate of excess carbon and nutrients in consumers. American Naturalist
165:1-15
Andersen T, Elser JJ, Hessen DO (2004) Stoichiometry and population dynamics.
Ecology Letters 7:884-900
Anderson TR, Hessen DO (1995) Carbon or nitrogen limitation in marine
copepods. Journal of Plankton Research 17:317-331
Andersen T, Hessen DO (1991) Carbon, nitrogen, and phosphorus content of
freshwater zooplankton. Limnology and Oceanography 36:807-814
Anderson WB, Mulder CPH (2011) An introduction to seabird islands. In: Mulder
CPH, Anderson WB, Towns DR, Bellingham PJ (eds) Seabird islands:
Ecology, invasion and restoration. Oxford University Press in press
Anderson WB, Polis GA (1999) Nutrient fluxes from water to land: seabirds affect
plant nutrient status on Gulf of California islands. Oecologia 118:324-332
Anderson WB, Polis GA (1998) Marine subsidies of island communities in the
Gulf of California: evidence from stable carbon and nitrogen isotopes. Oikos
81:75-80
Aneer G, Arvidsson D (2003) Inputs of nutrients (nitrogen and phosphorus) to
coastal waters of Svealand, northern Baltic Sea, in 1997 (in swedish with
english summary). Stockholm County Administrative Board Report 2003:17:
Barrett K, Anderson WB, Wait DA, Grismer LL, Polis GA, Rose MD (2005)
Marine subsidies alter the diet and abundance of insular and coastal lizard
populations. Oikos 109:145-153
Bedard J, Therriault JC, Berube J (1980) Assessment of the importance of nutrient
recycling by seabirds in the St Lawrence estuary. Canadian Journal of Fisheries
and Aquatic Sciences 37:583-588
Bird MI, Tait E, Wurster CM, Furness RW (2008) Stable carbon and nitrogen
isotope analysis of avian uric acid. Rapid Communications in Mass
Spectrometry 22:3393-3400
Blackburn TM, Cassey P, Duncan RP, Evans KL, Gaston KJ (2004) Avian
extinction and mammalian introductions on oceanic islands. Science 305:19551958
Blais JM, Kimpe LE, McMahon D, Keatley BE, Mattory ML, Douglas MSV,
Smol JP (2005) Arctic seabirds transport marine-derived contaminants. Science
309:445.
Blumenshine SC, Vadeboncoeur Y, Lodge DM, Cottingham KL, Knight SE
(1997) Benthic-pelagic links: responses of benthos to water-column nutrient
enrichment. Journal of the North American Benthological Society 16:466-479
64
Bosman AL, Dutoit JT, Hockey PAR, Branch GM (1986) A field experiment
demonstrating the influence of seabird guano on intertidal primary production.
Estuarine Costal and Shelf 23:283-294
Bosman AL, Hockey PAR (1986) Seabird guano as a determinant of rocky
intertidal community structure. Marine Ecology Progress Series 32:247-257
Brandvold DK, Popp CJ, Brierley JA (1976) Waterfowl refuge effect on waterquality.2. Chemical and physical parameters. Journal - Water Pollution Control
Federation 48:680-687
Brit VL, Brit TP, Goulet D, Cairnse DK, Montevecchi WA (1987) Ashmole`s
halo: direct evidence for prey depletion by seabirds. Marine Ecology Lake
Progress Series 40:205-208
Brown AC, McLachlan A (eds) (1990) Ecology of sandy shores. Elsevier,
Amsterdam, The Netherlands
Bultman TL, Uetz GW (1984) Effect of structure and nutritional quality of litter on
abundances of litter-dwelling arthropods. American Midland Naturalist
111:165-172
Burger AE, Lindeboom HJ, Williams AJ (1979) The mineral and energy
contributions of guano of selected species of birds to the Marion Island
terrestrial ecosystem. South African Journal of Antarctic Research 8:59-70
Carss DN (2002) Reducing the conflict between cormorants and fisheries on a
pan-European scale. Centre for Ecology & Hydrology Banchory, Hill of
Brathens, Banchory Aberdeenshire, AB 31 4BW, Scotland, UK
Chan EKW, Zhang YX, Dudgeon D (2009) Substrate availability may be more
important than aquatic insect abundance in the distribution of riparian orb-web
spiders in the tropics. Biotropica 41:196-201
Clesceri LS, Greenberg AE, Eaton AD (1998) Standard methods for the
examination of water and wastewater. American Pupblic Health Assoication,
NY
Cross WF, Benstead JP, Rosemond AD, Wallace JB (2003) Consumer-resource
stoichiometry in detritus-based streams. Ecology Letters 6:721-732
Croxall KH, Evans PGH, Schreiber RW (1984) Status and conservation of the
world's seabirds. International Council for Bird Preservation, Cambrig, UK
Cushman JH (1995) Ecosystem-level consequences of species additions and
deletions on islands. In: Vitousek PM, Loope LL, Adsersen H (eds) Biological
diversity and ecosystem function. Springer-Verlag, Berlin
Dalton CM, Ellis D, Post DM (2009) The impact of double-crested cormorant
(Phalacrocorax auritus) predation on anadromous alewife (Alosa
pseudoharengus) in south-central Connecticut, USA. Canadian Journal of
Fisheries and Aquatic Sciences 66:177-186
Darwin C (1959) The origin of species by means of natural selection of the
preservation of favoured races in the struggle for life. Signet Classic, London
DeMott WR, Pape BJ (2005) Stoichiometry in an ecological context: testing for
links between Daphnia P-content, growth rate and habitat preference.
Oecologia 142:20-27
65
Dennis P, Young MR, Gordon IJ (1998) Distribution and abundance of small
insects and arachnids in relation to structural heterogeneity of grazed,
indigenous grasslands. Ecological Entomology 23:253-264
Draulans D (1988) Effects of fish-eating birds on fresh-water fish stocks - an
evaluation. Biological Conservation 44:251-263
Ellis JC (2005) Marine birds on land: a review of plant biomass, species richness,
and community composition in seabird colonies. Plant Ecology 181:227-241
Ellis JC, Bellinham PJ, Cameron EK, Croll DA, Kolb GS, Kueffer C, Mittelhauser
GH, Schmidt S, Vidal E, Wait DA (2011) Effects of seabirds on plant
communities. In: Mulder CPH, Anderson WB, Towns DR, Bellingham PJ (eds)
Seabird islands: Ecology, invasion and restoration. Oxford University Press in
press
Ellis JC, Shulman MJ, Wood M, Witman JD, Lozyniak S (2007) Regulation of
intertidal food webs by avian predators on New England rocky shores. Ecology
88:853-863
Ellis JC, Farina JM, Witman JD (2006) Nutrient transfer from sea to land: the case
of gulls and cormorants in the Gulf of Maine. Journal of Animal Ecology
75:565-574
Elmgren R (2001) Understanding human impact on the Baltic ecosystem:
Changing views in recent decades. Ambio 30:222-231
Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai
JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and
phosphorus limitation of primary producers in freshwater, marine and terrestrial
ecosystems. Ecology Letters 10:1135-1142
Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S,
Fagan W, Schade J, Hood J, Sterner RW (2003) Growth rate-stoichiometry
couplings in diverse biota. Ecology Letters 6:936-943
Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison
JF, Hobbie SE, Odell GM, Weider LJ (2000a) Biological stoichiometry from
genes to ecosystems. Ecology Letters 3:540-550
Elser JJ, O'Brien WJ, Dobberfuhl DR, Dowling TE (2000b) The evolution of
ecosystem processes: growth rate and elemental stoichiometry of a key
herbivore in temperate and arctic habitats. Journal of Evolutionary Biology
13:845-853
Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling:
Theory, observations, and consequences. Ecology 80:735-751
Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH (1996) Organism size, life
history, and N:P stoichiometry. Bioscience 46:674-684
Elton C (1927) Animal ecology. MacMillan, New York, USA
Engstrom H (2001) Long term effects of cormorant predation on fish communities
and fishery in a freshwater lake. Ecography 24:127-138
Erskine PD, Bergstrom DM, Schmidt S, Stewart GR, Tweedie CE, Shaw JD
(1998) Subantarctic Macquarie Island - a model ecosystem for studying animalderived nitrogen sources using N15 natural abundance. Oecologia 117:187-193
66
Eyre MD, Luff ML (2005) The distribution of epigeal beetle (Coleoptera)
assemblages on the north-east England coast. Journal of Coastal Research
21:982-990
Fagan WF, Siemann E, Mitter C, Denno RF, Huberty AF, Woods HA, Elser JJ
(2002) Nitrogen in insects: Implications for trophic complexity and species
diversification. American Naturalist 160:784-802
Frank T, Reichhart B (2004) Staphylinidae and Carabidae overwintering in wheat
and sown wildflower areas of different age. Bulletin of Entomological
Research 94:209-217
Frost PC, Evans-White MA, Finkel ZV, Jensen TC, Matzek V (2005) Are you
what you eat? Physiological constraints on organismal stoichiometry in an
elementally imbalanced world. Oikos 109:18-28
Fukami T, Wardle DA, Bellingham PJ, Mulder CPH, Towns DR, Yeates GW,
Bonner KI, Durrett MS, Grant-Hoffman MN, Williamson WM (2006) Aboveand below-ground impacts of introduced predators in seabird-dominated island
ecosystems. Ecology Letters 9:1299-1307
Garcia RR, Jauregui BM, Garcia U, Osoro K, Celaya R (2009) Responses of
Arthropod Fauna Assemblages to goat grazing management in northern spanish
heathlands. Environmental Entomology 38:985-995
Gillham ME (1961) Alteration of breeding habitat by seabirds and seals in
Western Australia. The Journal of Ecology 49:289-300
Golovkin AN (1967) Effect of colonial sea birds on development of
phytoplankton. Oceanology-USSR 7:521-52&
Golovkin AN, Garkavaya GP (1975) Fertilization of waters off the Murmansk
coast by bird excreta near various types of colonies. Soviet Journal of Marine
Biology 1:345-351
Gratton C, Donaldson J, vander Zanden MJ (2008) Ecosystem linkages between
lakes and the surrounding terrestrial landscape in northeast Iceland. Ecosystems
11:764-774
Gremillet D, Argentin G, Schulte B, Culik BM (1998) Flexible foraging
techniques in breeding cormorants Phalacrocorax carbo and shags
Phalacrocorax aristotelis: benthic or pelagic feeding? IBIS 140:113-119
Grover JP (2003) The impact of variable stoichiometry on predator-prey
interactions: A multinutrient approach. American Naturalist 162:29-43
Haddad NM, Haarstad J, Tilman D (2000) The effects of long-term nitrogen
loading on grassland insect communities. Oecologia 124:73-84
Hahn S, Bauer S, Klaassen M (2007) Estimating the contribution of carnivorous
waterbirds to nutrient loading in freshwater habitats. Freshwater Biology
52:2421-2433
Hamback PA, Agren J, Ericson L (2000) Associational resistance: Insect damage
to purple loosestrife reduced in thickets of sweet gale. Ecology 81:1784-1794
Hansson S, Rudstam LG (1990) Eutrophication and baltic fish communities.
Ambio 19:123-125
Hart DD, Horwitz RJ (1991) Habitat diversity and species-area realtionship:
alternative modles and tests. In: Bell SS, McCoy ED, Mushinsky HR (eds)
67
Habitat structure: the pysical arrangment of objects in space. Chapman and
Hall, London
Hawke DJ, Clark JM (2010) Incorporation of the invasive mallow Lavatera
arborea into the food web of an active seabird island. Biological Invasions
12:1805-1814
Hebert CE, Duffe J, Weseloh DVC, Senese EMT, Haffner GD (2005) Unique
island habitats may be threatened by double-crested cormorants. Journal of
Wildlife Management 69:68-76
Hill C, Wallsröm K (2005) The Stockholm archipelago. In: Schiewer U (ed)
Ecology of baltic costal waters. Springer, Berlin, Heidelberg
Hobara S, Koba K, Osono T, Tokuchi N, Ishida A, Kameda K (2005) Nitrogen
and phosphorus enrichment and balance in forests colonized by cormorants:
Implications of the influence of soil adsorption. Plant and Soil 268:89-101
Hobara S, Osono T, Koba K, Tokuchi N, Fujiwara S, Kameda K (2001) Forest
floor quality and N transformations in a temperate forest affected by avianderived N deposition. Water, Air, and Soil Pollution 130:679-684
Hunter MD (2003) Effects of plant quality on the population ecology of
parasitoids. Agricultural and Forest Entomology 5:1-8
Hunter MD, Price PW (1992) Playing chutes and ladders - heterogeneity and the
relative roles of bottom-up and top-down forces in natural communities.
Ecology 73:724-732
Hurd LE, Fagan WF (1992) Cursorial spiders and succession - age or habitat
structure. Oecologia 92:215-221
Iason GR, Duck CD, Cluttonbrock TH (1986) Grazing and reproductive success of
red deer - the effect of local enrichment by gull colonies. Journal of Animal
Ecology 55:507-515
Ishida A (1996) Effects of the common cormorant, Phalacrocorax carbo, on
evergreen forests in two nest sites at Lake Biwa, Japan. Ecological Rearch
11:193-200
Jacobs W, Renner M (1998) Biologie und Ökologie der Insekten (in german) (3.
Auflage). Gustav Fischer, Stuttgard
Joern A, Behmer ST (1997) Importance of dietary nitrogen and carbohydrates to
survival, growth, and reproduction in adults of the grasshopper Ageneotettix
deorum (Orthoptera: Acrididae). Oecologia 112:201-208
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers.
Oikos 69:373-386
Jones HP (2010) Prognosis for ecosystem recovery following rodent eradication
and seabird restoration in an island archipelago. Ecological Applications
20:1204-1216
Jones HP, Tershy BR, Zavaleta ES, Croll DA, Keitt BS, Finkelstein ME, Howald
GR (2008) Severity of the effects of invasive rats on seabirds: A global review.
Conservation Biology 22:16-26
Kagata H, Ohgushi T (2006) Nitrogen homeostasis in a willow leaf beetle,
Plagiodera versicolora, is independent of host plant quality. Entomologia
Experimentalis et Applicata 118:105-110
68
Kautsky L, Norbeg Y, Aneer G, Engqvist A (2000) Under the surface of the
Stockholm Archipelago (in swedish) County Administrative Board. Lenanders
Tryckeri of Stockholm, Sweden
Kautsky H, Kautsky L, Kautsky N, Kautsky U, Lindblad C (1992) Studies on the
Fucus vesiculosus community in the Baltic sea. Acta Phytogeographica Suecica
88:33-48
Kay AD, Rostampour S, Sterner RW (2006) Ant stoichiometry: elemental
homeostasis in stage-structured colonies. Functional Ecology 20:1037-1044
Keatley B, Douglas M, Blais JM, Mallory M, Smol J (2009) Impacts of seabirdderived nutrients on water quality and diatom assemblages from Cape Vera,
Devon Island, Canadian High Arctic. Hydrobiologia 621:191-205
Kolb GS, Young HS, Anderson WB (2011) Effects of seabirds on island
consumers. In: Mulder CPA, Anderson WB, Towns DR, Belligham PJ (eds)
Seabird islands: Ecology, invasion, and restoraition. Oxford University Press in
press
Kooijman SALM (1995) The stoichiometry of animal energetics. Journal of
Theoretical Biology 177:139-149
Kotta J, Paalme T, Martin G, Makinen A (2000) Major changes in macroalgae
community composition affect the food and habitat preference of Idotea
baltica. International Reviwe if Hyrrobiology 85:697-705
Kraufvelin P (2007) Responses to nutrient enrichment, wave action and
disturbance in rocky shore communities. Aquatic Botany 87:262-274
Kraufvelin P, Salovius S, Christie H, Moy FE, Karez R, Pedersen MF (2006)
Eutrophication-induced changes in benthic algae affect the behaviour and
fitness of the marine amphipod Gammarus locusta. Aquatic Botany 84:199-209
Kurle CM, Croll DA, Tershy BR (2008) Introduced rats indirectly change marine
rocky intertidal communities from algae- to invertebrate-dominated.
Proceedings of the National Academy of Sciences of the United States of
America 105:3800-3804
Kyto M, Niemela P, Larsson S (1996) Insects on trees: Population and individual
response to fertilization. Oikos 75:148-159
Lapointe BE, Litter MM, Litter DS (1992) Modification of benthic community
structure by natural eutrophication: the Belize Barrier Reef. Proceedings of the
Seventh International Coral Reef Symposium 1
Lindeboom (1984) The nitrogen pathway in a penguin rookery. Ecology 65:269277
Linderholm J (2007) Soil chemical surveying: A path to a deeper understanding of
prehistoric sites and societies in Sweden. Geoarchaeology an International
Journal 22:417-438
Littler MM, Littler DS, Titlyanov EA (1991) Comparisons of N-limited and Plimited productivity between high granitic islands versus low carbonate atolls
in the seychelles archipelago - a test of the relative-dominance paradigm. Coral
Reef 10:199-209
69
Loder TC, Ganning B, Love JA (1996) Ammonia nitrogen dynamics in coastal
rockpools affected by gull guano. Journal of Experimental Marine Biology and
Ecology 196:113-129
Logan JD, Joern A, Wolesensky W (2004) Control of CNP homeostasis in
herbivore consumers through differential assimilation. Bulletin of
Mathematical Biology 66:707-725
Lomolino MV, Riddle BR, Brown JH (2006) Biogeography.
Lopez-Victoria M, Wolters V, Werding B (2009) Nazca Booby (Sula granti)
inputs maintain the terrestrial food web of Malpelo Island. Journal für
Ornithologie 150:865-870
MacArthur RH, Wilson EO (1963) Equilibrium-theory of insular zoogeography.
Evolution; International Journal of Organic Evolution 17:373-37
MacArthur R, MacArthur JW (1961) On bird species-diversity. Ecology 42:59459
Marczak LB, Richardson JS (2007) Spiders and subsidies: results from the riparian
zone of a coastal temperate rainforest. Journal of Animal Ecology 76:687-694
Marczak LB, Thompson RM, Richardson JS (2007) Meta-analysis: Trophic level,
habitat, and productivity shape the food web effects of resource subsidies.
Ecology 88:140-148
Marion L, Clergeau P, Brient L, Bertru G (1994) The importance of aviancontributed nitrogen (N) and phosphorus (P) to Lake Grand-Lieu, France.
Hydrobiologia 280:133-147
Markwell TJ, Daugherty CH (2002) Invertebrate and lizard abundance is greater
on seabird-inhabited islands than on seabird-free islands in the Marlborough
Sounds, New Zealand. Ecoscience 9:293-299
Maron JL, Estes JA, Croll DA, Danner EM, Elmendorf SC, Buckelew SL (2006)
An introduced predator alters Aleutian Island plant communities by thwarting
nutrient subsidies. Ecological Monographs 76:3-24
Mattson WJ (1980) Herbivory in relation to plant nitrogen-content. Annual
Review of Ecology and Systematics 11:119-161
Mayntz D, Toft S (2001) Nutrient composition of the prey's diet affects growth
and survivorship of a generalist predator. Oecologia 127:207-213
McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic
shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378390
Mellbrand K, Hambäck PA (2011). Coastal niches for prdators: a stable isotope
study. Canadian Journal of Zoology in press
Mitchell RJ (1992) Testing evolutionary and ecological hypotheses using pathanalysis and structural equation modeling. Functional Ecology 6:123-129
Mittelbach GG, Steiner CF, Scheiner SM, Gross KL, Reynolds HL, Waide RB,
Willig MR, Dodson SI, Gough L (2001) What is the observed relationship
between species richness and productivity? Ecology 82:2381-2396
Miyashita T, Takada M (2007) Habitat provisioning for aboveground predators
decreases detritivores. Ecology 88:2803-2809
70
Mizutani H, Hasegawa H, Wada E (1986) High nitrogen isotope ratio for soils of
seabird rookeries. Biochemistry 2:221-247
Mizutani H, Wada E (1988) Nitrogen and carbon isotope ratios in seabird
rookeries and their ecological implications. Ecology 69:340-349
Mulder C, Elser JJ (2009) Soil acidity, ecological stoichiometry and allometric
scaling in grassland food webs. Gloabal Change Biology 15:2730-2738
Mulder CPH, Jones H, Kameda K, Palmborg C, Schmidt S, Ellis JC, Orrock JL,
Wait DA, Wardle DE, Yang L, Young H, Croll D, Vidal E (2011) Impacts of
seabirds on plant and soil properties. In: Mulder CPH, Anderson WB, Towns
DR, Bellingham PJ (eds) Seabird islands: ecology, invasion and restoration.
Oxford University Press in press
Mulder K, Bowden WB (2007) Organismal stoichiometry and the adaptive
advantage of variable nutrient use and production efficiency in Daphnia.
Ecological Modelling 202:427-440
Nakano S, Murakami M (2001) Reciprocal subsidies: Dynamic interdependence
between terrestrial and aquatic food webs. Proceedings of the National
Academy of Sciences of the United States of America 98:166-170
Onuf CP, Teal JM, Valiela I (1977) Interactions of Nutrients, Plants Growth and
Herbivory in a Mangrove Ecosystem. Ecology 58:514-526
Orav-Kotta H, Kotta J (2004) Food and habitat choice of the isopod Idotea baltica
in the northeastern Baltic Sea. Hydrobiologia 514:79-85
Orgeas J, Vidal E, Ponel P (2003) Colonial seabirds change beetle assemblages on
a Mediterranean Island. Ecosience 10:38-44
Osono T, Hobaraa S, Fujiwaraa S, Kobab K, Kamedac K (2002) Abundance,
diversity, and species composition of fungal communities in a temperate forest
affected by excreta of the Great Cormorant Phalacrocorax carbo. Soil Biology
& Biochemistry 34: 1537-1547
Paetzold A, Lee M, Post DM (2008) Marine resource flows to terrestrial arthropod
predators on a temperate island: the role of subsidies between systems of
similar productivity. Oecologia 157:653-659
Paillisson JM, Carpentier A, Le Gentil J, Marion L (2004) Space utilization by a
cormorant (Phalacrocorax carbo L.) colony in a multi-wetland complex in
relation to feeding strategies. Comptes Rendus Biologies 327:493-500
Palomo G, Iribarne O, Martinez MM (1999) The effect of migratory seabirds
guano on the soft bottom community of a SW Atlantic coastal lagoon. Bulletin
of Marine Science 65:119-128
Perner J, Voigt W, Bahrmann R, Heinrich W, Marstaller R, Fabian B, Gregor K,
Lichter D, Sander FW, Jones TH (2003) Responses of arthropods to plant
diversity: changes after pollution cessation. Ecography 26:788-78
Persson J, Fink P, Goto A, Hood JM, Jonas J, Kato S (2010) To be or not to be
what you eat: regulation of stoichiometric homeostasis among autotrophs and
heterotrophs. Oikos 119:741-751
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annual Review of
Ecology and Systematics 18:293-320
71
Polis GA, Sáchez-Piñero F, Stapp PT, Anderson WB, Rose MR (2004) Trophic
flows from water to land: marine input affects food webs of island and costal
ecosystems worldwide. Food webs at the landescape level. The University of
Chicago Press Chicago and London
Polis GA, Hurd SD, Jackson CT, Pinero FS (1997a) El Nino effects on the
dynamics and control of an island ecosystem in the Gulf of California. Ecology
78:1884-1897
Polis GA, Anderson WB, Holt RD (1997b) Toward an integration of landscape
and food web ecology: The dynamics of spatially subsidized food webs.
Annual Review of Ecology and Systematics 28:289-316
Polis GA, Hurd SD (1996a) Linking marine and terrestrial food webs:
Allochthonous input from the ocean supports high secondary productivity on
small islands and coastal land communities. American Naturalist 147:396-423
Polis GA, Hurd SD (1996b) Linking marine and terrestrial food webs:
Allochthonous input from the ocean supports high secondary productivity on
small islands and coastal land communities. American Naturalist 147:396-423
Polis GA, Hurd SD (1995) Extraordinarily high spider densities on islands - flow
of energy from the marine to terrestrial food webs and the absence of predation.
Proceedings of the National Academy of Sciences of the United States of
America 92:4382-4386
Ponsard S, Averbuch P (1999) Should growing and adult animals fed on the same
diet show different delta N-15 values? Rapid Communications in Mass
Spectrometry 13:1305-1310
Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG
(2007) Getting to the fat of the matter: models, methods and assumptions for
dealing with lipids in stable isotope analyses. Oecologia 152:179-189
Power ME, Huxel GR (2004) preface. In: Polis GA, Power ME, Huxel GR (eds)
Food webs at the landscape level. The University of Chicago Press, Chicago
and London
Price PW (2002) Resource-driven terrestrial interaction webs. Ecological research
17:241-247
Råberg S, Kautsky L (2007) A comparative biodiversity study of the associated
fauna of perennial fucoids and filamentous algae. Estuarine Costal and Shelf
Science73:249-258
Råberg S, Kautsky L (2008) Grazer identity is crucial for facilitating growth of the
perennial brown alga Fucus vesiculosus. Marine Ecology Progress Series
361:111-118
Raubenheimer D, Jones SA (2006) Nutritional imbalance in an extreme generalist
omnivore: tolerance and recovery through complementary food selection.
Animal Behaviour 71:1253-1262
Raubenheimer D, Simpson SJ (2004) Organismal stoichiometry: Quantifying nonindependence among food components. Ecology 85:1203-1216
Rolland C, Danchin E, de Fraipont M (1998) The evolution of coloniality in birds
in relation to food, habitat, predation, and life-history traits: A comparative
analysis. American Naturalist 151:514-529
72
Root RB (1973) Organization of a plant-arthropod association in simple and
diverse habitats - fauna of collards (Brassica oleracea). Ecological
Monographs 43:95-120
Ryan PG, Watkins BP (1989) The influence of physical factors and ornithogenic
products on plant and arthropod abundance at an inland Nunatak group in
Antarctica. Polar Biology 10:151-160
Sanchez-Pinero F, Polis GA (2000) Bottom-up dynamics of allochthonous input:
Direct and indirect effects of seabirds on islands. Ecology 81:3117-3132
Schmidt MH, Clough Y, Schulz W, Westphalen A, Tscharntke T (2006) Capture
efficiency and preservation attributes of different fluids in pitfall traps. Journal
of Arachnology
Schmidt S, Dennison WC, Moss GJ, Stewart GR (2004) Nitrogen ecophysiology
of Heron Island, a subtropical coral cay of the Great Barrier Reef, Australia.
Functional plant biology 31:517-528
Siemann E (1998) Experimental tests of effects of plant productivity and diversity
on grassland arthropod diversity. Ecology 79:2057-2070
Siemann E, Tilman D, Haarstad J, Ritchie M (1998) Experimental tests of the
dependence of arthropod diversity on plant diversity. American Naturalist
152:738-750
Sinclair BJ, Chown SL (2006) Caterpillars benefit from thermal ecosystem
engineering by wandering albatrosses on Sub-Antarctic Marion Island. Biology
Letters 2:51-54
Slansky F, Feeny P (1977) Stabilization of rate of nitrogen accumulation by larvae
of cabbage butterfly on wild and cultivated food plants. Ecological
Monographs 47:209-228
Small GE, Pringle CM (2010) Deviation from strict homeostasis across multiple
trophic levels in an invertebrate consumer assemblage exposed to high chronic
phosphorus enrichment in a Neotropical stream. Oecologia 162:581-590
Smith JL, Mulder CPH, Ellis JC (2011) Seabirds as engineers: Nutrient inputs and
physical disturbance. In: Mulder CPH, Anderson WB, Towns DR, Bellingham
PJ (eds) Seabird islands: Ecology, invasion and restoration. Oxford University
Press in press
Smith JS, Johnson CR (1995) Nutrient inputs from seabirds and humans on a
populated coral cay. Marine Ecology Progress Series 124:189-200
Sobey DG, Kenworthy JB (1979) Relationship between herring-gulls and the
vegetation of their breeding colonies. Journal of Ecology 67:469-496
Spiller DA, Schoener TW (1994) Effects of top and intermediate predators in a
terrestrial food-web. Ecology 75:182-196
Spiller DA, Schoener TW (1997) Folivory on islands with and without
insectivorous lizards: An eight-year study. Oikos 78:15-22
Staav R (2010) Skarv (in swedish). In: Strandfager K, Palmblad U (eds) Levande
skärgårdsnatur 2010 - med rapporter från 2009. Skärgårdsstiftelsen, Stockholm
Staav R (2008) Skarv (in swedish). In: Strandfager K, Palmblad U (eds) Levande
skärgårdsnatur 2008 - med rapporter från 2007. Skärgårdsstiftelsen, Stockholm
73
Stapp P, Polis GA (2003) Marine resources subsidize insular rodent populations in
the Gulf of California, Mexico. Oecologia 134:496-504
Sterner RW, Elser JJ (2002) Ecological Stoichiometry. The biology of elements
from molecules to the biosphere. Princeton University Press, Princeton, New
Jersey, UK
Sterner RW, Schwalbach MS (2001) Diet integration of food quality by Daphnia:
Luxury consumption by a freshwater planktonic herbivore. Limnology and
Oceanography 46:410-416
Sterner RW, Elser JJ, Hessen DO (1992) Stoichiometric relationships among
producers, consumers and nutrient cycling in pelagic ecosystems. Biochemistry
17:49-67
Thingstad TF (1987) Utilization of N, P, and organic C by heterotrophic
bacteria.1. Outline of a chemostat theory with a consistent concept of
maintenance metabolism. Marine Ecology Progress Series 35:99-109
Tilman D (1987) The importance of the mechanisms of interspecific competition.
American Naturalist 129:769-774
Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by
biodiversity in grassland ecosystems. Nature 379:718-720
Towns DR, Wardle DA, Mulder CPH, Yeates GW, Fitzgerald BM, Parrish GR,
Bellingham PJ, Bonner KI (2009) Predation of seabirds by invasive rats:
multiple indirect consequences for invertebrate communities. Oikos 118:420430
Urabe J, Kyle M, Makino W, Yoshida T, Andersen T, Elser JJ (2002) Reduced
light increases herbivore production due to stoichiometric effects of
light/nutrient balance. Ecology 83:619-627
Urabe J, Watanabe Y (1992) Possibility of N-limitation or P-limitation for
planktonic cladocerans - an experimental test. Limnology and Oceanography
37:244-251
Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet delta N15 enrichment: a meta-analysis. Oecologia 136:169-182
Vanni MJ (2002) Nutrient cycling by animals in freshwater ecosystems. Annual
Review of Ecology and Systematics 33:341-370
Vitousek PM, Adsersen H, Loope LL (1995) Introduction - Why focus on islands?
In: Vitousek PM, Loope LL, Andersen H (eds) Islands: biological diversity and
ecosystem function. Springer-Verlag, Berlin
Voss M, Deutsch B, Elmgren R, Humborg C, Kuuppo P, Pastuszak M, Rolff C,
Schulte U (2006) Source identification of nitrate by means of isotopic tracers in
the Baltic Sea catchments. Biogeoscienc 3:663-676
Waide RB, Willig MR, Steiner CF, Mittelbach G, Gough L, Dodson SI, Juday GP,
Parmenter R (1999) The relationship between productivity and species
richness. Annual Review of Ecology and Systematics 30:257-300
Wainright SC, Haney JC, Kerr C, Golovkin AN, Flint MV (1998) Utilization of
nitrogen derived from seabird guano by terrestrial and marine plants at St. Paul,
Pribilof Islands, Bering sea, Alaska. Marine Biology 131:63-71
74
Wait DA, Aubrey DP, Anderson WB (2005) Seabird guano influences on desert
islands: soil chemistry and herbaceous species richness and productivity.
Journal of Arid Enviroments 60:681-695
Wardle DA, Bellingham PJ, Fukami T, Mulder CPH (2007) Promotion of
ecosystem carbon sequestration by invasive predators. Biology Letters 3:479482
Wardle DA, Bonner KI, Nicholson KS (1997) Biodiversity and plant litter:
Experimental evidence which does not support the view that enhanced species
richness improves ecosystem function. Oikos 79:247-258
Wheeler GS, Halpern MD (1999) Compensatory responses of Samea multiplicalis
larvae when fed leaves of different fertilization levels of the aquatic weed Pistia
stratiotes. Entomologia Experimentalis et Applicata 92:205-216
White TCR (1993) The Inadequate Environment: Nitrogen and the Abundance of
Animals.
Whittaker RJ, Heegaard E (2003) What is the observed relationship between
species richness and productivity? comment. Ecology 84:3384-3390
Wikstrom SA, Kautsky L (2007) Structure and diversity of invertebrate
communities in the presence and absence of canopy-forming Fucus vesiculosus
in the Baltic Sea. Estuarine Coastal and Shelf Science 72:168-176
Wolfe KM, Mills HR, Garkaklis MJ, Bencini R (2004) Post-mating survival in a
small marsupial is associated with nutrient inputs from seabirds. Ecology
85:1740-1746
Wootton JT (1992) Indirect effects, prey susceptibility, and habitat selection impacts of birds on limpets and algae. Ecology 73:981-991
Wootton JT (1991) Direct and indirect effects of nutrients on intertidal community
structure - variable consequences of seabird guano. Journal of Experimental
Marine Biology and Ecology 151:139-153
Worm B, Lotze HK, Sommer U (2000) Coastal food web structure, carbon
storage, and nitrogen retention regulated by consumer pressure and nutrient
loading. Limnology and Oceanography 45:339-349
Worm B, Sommer U (2000) Rapid direct and indirect effects of a single nutrient
pulse in a seaweed-epiphyte-grazer system. Marine Ecology Progress Series
202:283-288
Wright DG, van der Wal R, Wanless S, Bardgett RD (2010) The influence of
seabird nutrient enrichment and grazing on the structure and function of island
soil food webs. Soil Biology and Biochemistry 42:592-600
Wright A (1934) The method of path coefficients. Annals of Mathematics and
Statistics 5:161-215
Young HS, Hurrey L, Kolb GS (2011) Effects of seabird-derived nutrients on
aquatic systems. In: Mulder CPH, Anderson WB, Towns DR, Bellingham PJ
(eds) Seabird islands: Ecology, invasion and restoration. Oxford University
Press. in press
Zelickmaea, Golovkin AN (1972) Composition, structure and productivity of
neritic plankton communities near bird colonies of northern shores of Nnovaya
Zemlya. Marine Biology 17:265-26
75
Svensk sammanfattning
Den här avhandlingen handlar om hur skarvkolonier påverkar dels växter och
leddjur (insekter, spindlar och kräftdjur) på häckningsöar och dels alger och
associerade ryggradslösa djur omkring öarna. Jag har använt mig av så kallad
stabil isotopanalys (kol och kväve) för att följa resan av kväve från skarvarna
genom näringsvävarna på öarna och i närliggande vatten. Jag undersökte hur
individantal, artrikedom och artsammansättning av växter och djur förändras av
skarvarnas närvaro, genom att jämföra öar med häckande skarv med öar utan.
Dessutom undersökte jag näringsinnehållet i djuren och deras förmåga att hålla
kol:kväve:fosfor (C:N:P) proportionerna konstanta (homeostatis) och testade om
skillnader i näringsinnehåll och homeostasis kan förklara hur individantal av de
olika taxonomiska grupperna ändrade sig under påverkan.
Skarvar är fiskätande sjöfåglar som häckar i kolonier upp till 10 000 par. De
har återkoloniserat Stockholms skärgård sedan 1994 och deras antal ökade fram till
2007. Därefter verkar populationsstorleken ha stabiliserat sig på omkring 5200 par
fördelat på 20 kolonier. Det finns en stor svensk opinion som ogillar skarvens
återkomst i svensk natur och anser att skarven påverkar skärgårdens ekosystem
negativt. Argumenten för detta är att skarven konsumerar stora mängder fisk samt
förstör naturen vid häckningsöarna. Konstigt nog har ingen vetenskaplig
undersökning gjorts för att utreda hur skarvarna påverkar skärgårdens ekosystem,
och detta är mig veterligen den första studien.
Skarvar transporterar, liksom andra fiskätande sjöfåglar, näring från vattnet till
land. De jagar fisk inom ett stort område och häckar eller vilar på land, ofta på öar,
där de lämnar stora mängden av näringsrik spillning (guano), kadaver, döda fiskar
och äggskal. Detta näringsbidrag gödslar jorden och ökar näringsinnehållet i
växterna, samt förändrar växternas artsammansättning och minskar antalet arter.
Dessutom gynnas många leddjur direkt eller indirekt av skarv, genom att dels
konsumera det som skarvarna lämnar efter sig och dels genom växternas ökade
näringsinnehåll. Individantalet av leddjur ökar därför ofta på skarvöar men den
minskade artrikedomen av växter reducerar också artantalet av växtätare. Näringen
från fågelspillning påverkar inte bara ekosystemet på öarna utan även genom
avrinning ekosystemet i det närbelägna vattnet. Ökade närsaltskoncentrationer i
vattnet kan påverka vattenlevande organismer på motsvarande sätt som på land.
En gren inom ekologin som kallas ekologisk stökiometri har skapat en teoretisk
ram för relationen mellan artegenskaper, näringsbehov och populationstillväxt.
Många tillväxtmodeller är byggda på antagande att djur håller kvoten C:N:P
konstant oberoende av näringsinnehållet i sin föda (homeostas), i motsats till
växter. Senare studier har dock visat att inte alla djur är strängt homeostatiska. Jag
antog att djur som inte är homeostatiska kan dämpa förändringar i näringsinnehållet av sin föda och därför visa mindre skillnader i individantal mellan skarv
och icke-skarv öar. Tidigare studier tyder på att djurens C:N:P-kvot bestämmer
deras näringsbehov. Näringsrika djur behöver mer näringsämnen och är känsligare
76
för att bli begränsade av näringsämnen än näringsfattiga djur. Därför borde
näringsrika djur påverkas mer positivt av skarvödsling och visa starkare ökning i
individantal på skarvöar än näringsfattiga djur.
Jag observerade, liksom tidigare studier på fågelöar, att kväve och fosfatinnehållet i växter var högre, medan vegetationens täckningsgrad och artrikedomen var lägre på skarvöar än på icke-skarvöar. På övergivna skarvöar var
artrikedomen lika hög som på icke-skarvöar, men växtbiomassan tenderade att
vara högre.,
Artsammansättningen av växter skilde sig mellan skarv och icke-skarvöar, men
var lika mellan övergivna skarvöar och icke-skarvöar. Några, men inte alla,
grupper av ryggradslösa djur reagerade på skarvnärvaro genom förändringar i
individantal, artrikedom och artsammansättning. De kvantitativa förändringarna
kunde vara både positiva och negativa. Några växtätare, svampätare och kadaverätare blev positivt påverkade av förhöjd födokvalitet eller kvantitet och ökade i
individ- eller artantal. Andra växtätande, detritusätande och rovlevande djurgrupper missgynnades av förändringarna i vegetationsstruktur och jordkemi och
var på skarvöar mindre individ- eller artrika än på icke-skarvöar. Skillnaden i
förändringar av individantal mellan taxonomiska grupper kunde inte förklaras av
skillnader i djurens näringsinnehåll, i motsats till mitt antagande. Jag fann vidare
inget samband mellan homeostasnivån och den observerade förändringen i
individantal mellan djurgrupper.
Vill man avgöra om skarvkolonierna ökar eller minskar artrikedom måste man
skilja mellan lokal artrikedom (=artrikedom på en ö) och regional artrikedom
(=artrikedom i ett skärgårdsområde). Även om skarvar kan minska artrikedom av
växter och några leddjursgrupper på häckningsöarna, ökar de också den regionala
habitatheterogeniteten, genom att ändra artsammansättningen hos växterna,
jordkemi, vegetationsstruktur och resurstillgång. På grund av en ökad
habitatheterogenitet kan den regionala artrikedomen öka eftersom olika arter trivs i
olika habitat.
En viktig observation i mitt arbete är vidare den täta kopplingen mellan
näringsväven på land och den i vattnet. Genom att fjädermyggor som har
larvstadier i vatten och vuxenstadier på land och marina alger spolas upp på land
blir föda åt landlevande djur kopplas näringsvävarna ihop. Analyser av stabila
isotoper har visat att fjädermyggor är en mycket viktig resurs för spindlar och
några rovinsekter på land och detta öppnar möjligheten för en återkoppling mellan
ekosystemet på land och det i vattnet. Dessutom indikerade den stabila
isotopanalysen att näring från skarvspillningen rann ned från öarna till omgivande
vatten, att denna näring togs upp av alger och sedan fortsatte upp i näringsväven
till växtätande ryggradslösa djur. Ökade närsaltskoncentrationer stimulerande
produktionen av påväxtalger vilket ledde till högre biomassa av några djurgrupper,
däribland fjädermyggslarver. Ökad biomassa av vuxna fjädermyggor som flyger in
över land återkopplar därmed till näringsväven på land. Mina studier visade inte att
den lokalt ökade närsaltskoncentrationen runt skarvöarna främjar övergödningen
av Östersjön. Tvärtom tar skarvarna upp näring från vattnet (fiskar) och
77
transporterar denna till land, och endast en liten del av denna näring rinner tillbaka
till vattnet.
78
TACK!
När jag började min doktorandtjänst trodde jag att fyra år var en ganska lång tid
men de fyra år rasade förbi tack vare ett omväxlande arbete i fält, i laboratoriet och
framför dator, artikel- och bokläsning, kurser, möten och doktorandresor. Under
dessa år som doktorand har jag lärt mig många saker; att fika är mycket viktigt i
Sverige, att allt tar längre tid än man tror, att det kan vara bra att tänka efter lite
innan man gör något (och även innan man säger något), att man kan skriva om ett
stycke 1000 gånger och att det ändå inte blir bra, att fältdata och statistik inte alltid
går bra ihop, att man ska spara noga och regelbundet, att ett litteraturprogram
kanske inte är så dumt, att man ska ha ett system in sina datorfiler (det vill säga ett
bra system), att man inte bör ta kritik på sin arbete personligt, att åka båt inte är
detsamma som att åka bil, att abborre och sill smaka faktisk bra. (Självklart lärde
jag mig också mycket om forskning, metoder, teorier, statistik, planering och
sådant). Men framför allt gav mig min doktorandtjänst möjligheten att upptäckta
hur fantastiskt vacker Stockholms skärgård är, hur olika den kan se ut beroende på
vädret och årstid och det är jag mycket glad över.
Alla dessa lärorika år hade jag många hjälpsamma människor på min sida och utan
dem skulle jag aldrig ha klarar att genom- och slutföra min avhandling. Alla dessa
människor vill jag passa på att tacka här. Först vill jag tacka min handledare Peter,
för att du ordnade med resurser så att jag kunde genomföra mitt projekt, hade
assistenter och kunde åka på konferenser och kurser. Tack för att du gav mig
mycket frihet i mitt fältarbete och tidsplaneringen, tack för att du alltid läste mina
texter så snabb utan att tröttna, tack för att du hjälpte mig med statistiken,
vetenskapliga och språkliga frågor och tack att jag fick ringa dig även på helgen
eller under din semester. Tack även min biträdande handledare Lenn och hela
familjen Jerling (samt Eva) för underbara somrar på Norröra som jag redan har
börjat att sakna och som jag aldrig kommer att glömma., Tack för båtkörning (utan
er skulle hela projektet aldrig ha fungerat), assistans i fält, matlagning, diskning,
tömma dassen (Bitte). Tack för trevligt sällskap och för att ni alltid fick mig att
känna mig välkommen på ert sommarställe! Tack Lenn för att ta hand om båten,
berätta så mycket om skärgården och tack för ett kram och uppmuntrande ord när
det behövdes.
Tacka vill jag också alla mina doktorandkolleger på Botan för en bra stämning,
bokdiskussioner och hjälp när man behövde det. Framförallt tackar jag min
rumskompis Martin; utan dig skulle de fyra åren ha varit så mycket tristare.0 Tack
för allt vetenskapligt och privat utbyte och för att du lyssnade på mina utbrott.
Tack också till dig Jocke, för din hjälp och för att lyssna, särskilt i början och nu
på slutet av doktorandtiden. Tack Johan D. för statistiskhjälp. Tack Didrik för
uppmuntrande ord. Tack Kajsa för hjälp i fält. Tack Petter för roliga samtal. Tack
Tove för hjälpen med engelskan. Bryndis för din energi. Tack Helena för
virkningstips. Tack alla doktorander som var med i Spanien på två roliga resor.
Tack Sonja för hjälpen med Fucus-frågor.
79
Ett stort tack också till mina fält- och labassistenter Maria, Hanna, Annika och
Caroline för allt utmärkt jobb ni har gjort och trevligt sällskap ni har varit på
Norröra och på Botan. Tack också till dig Jessica för att jag alltid har kunnat fråga
dig om hjälp och prata några ord. Tack Sofia för hjälpen men paper III. Tack
Kristoffer för hjälpen med paper II. Tack Johan E. för att vara trevlig och roande.
Tack Cissi för jorddata. Mitt tack gäller även den övriga personalen på Botan; tack
Peter och Ingela för att ni tagit hand om mina fackelblomster och för att gestalta så
fina rabatter att jag alltid blir glad när jag kommer till jobbet. Tack Johan K. för
datorsupporten. Tack Ahmed för att städa och alltid le när man ser dig. Tack till
den administrativa personalen och tack Gisela för all hjälp när jag började på
Botan.
Thanks also to the SEAPRE network for inspiring meetings and real interest in my
work.
But I would have never been able to do a PhD if my parents wouldn`t have paid
me my education: Vielen lieben Dank Mama und Papa für die Finanzierung
meines Studiums und seelische Unterstützung. Und auch Dir Oma Friedel vielen
lieben Dank. Danke auch Euch meinen Freunden in Deutschland für Besuche,
Telefonate, mails och Skypsupport .
Tack min svenska familj och alla mina svenska vänner som gör att jag känner mig
hemma i Sverige och visar mig vad det är som är verkligen är viktig i livet.
Sist men inte minst vill jag tacka dig min älskade Magnus. Tack att du stod ut med
mig under dem senaste veckorna, att du lyssna på mitt gnäll och tack för all
assistans i fält. Tack att du finns, utan dig vore mitt liv så mycket fattigare.
80