The authors have declared that no competing interests exist.
Conceived and designed the experiments: GK. Performed the experiments: GK. Analyzed the data: GK. Contributed reagents/materials/analysis tools: GK CP. Wrote the paper: GK CP PH.
Seabirds deposit large amounts of nutrient rich guano on their nesting islands. The increased nutrient availability strongly affects plants and consumers. Consumer response differs among taxonomic groups, but mechanisms causing these differences are poorly understood. Ecological stoichiometry might provide tools to understand these mechanisms. ES suggests that nutrient rich taxa are more likely to be nutrient limited than nutrient poorer taxa and are more favored under nutrient enrichment. Here, we quantified differences in the elemental composition of soil, plants, and consumers between islands with and without nesting cormorant colonies and tested predictions made based on ES by relating the elemental composition and the eventual mismatch between consumer and resource stoichiometry to observed density differences among the island categories. We found that nesting cormorants radically changed the soil nutrient content and thereby indirectly plant nutrient content and resource quality to herbivores. In contrast, consumers showed only small differences in their elemental composition among the island categories. While we cannot evaluate the cause of the apparent homeostasis of invertebrates without additional data, we can conclude that from the perspective of the next trophic level, there is no difference in diet quality (in terms of N and P content) between island categories. Thus, bottom-up effects seemed mainly be mediated via changes in resource quantity not quality. Despite a large potential trophic mismatch we were unable to observe any relation between the invertebrate stoichiometry and their density response to nesting cormorant colonies. We conclude that in our system stoichiometry is not a useful predictor of arthropod responses to variation in resource nutrient content. Furthermore, we found no strong evidence that resource quality was a prime determinant of invertebrate densities. Other factors like resource quantity, habitat structure and species interactions might be more important or masked stoichiometric effects.
Seabirds strongly affect the nutrient pools on their nesting islands by depositing huge amounts of nitrogen and phosphorus rich guano
Herbivores and plant feeding detritivores, especially, face the problem of a fundamental mismatch between the elemental composition of their body tissues and their resources; consequently nutrient limitation seem to be common in herbivore and detritivore populations
Predicting the effect of nutrient additions on the density of specific taxa is fraught with difficulties not only because of trophic feedbacks
ES assumes that taxon-dependent differences in elemental composition determine differences in nutrient demand among species
In this study, we tested these possibilities on a set of islands with and without cormorant colonies in the Stockholm archipelago, Sweden. The effects of cormorant colonies on island vegetation, density and species composition of island arthropods, and near-shore algae and their associated invertebrates were reported in three previous studies
Sampling took place on and nearby islands in the Stockholm archipelago, Sweden (N 59° 20′ E 18° 03′) in summer 2007–2009. The archipelago consists of about 24 000 islands whose sizes vary between less than one m2 and several km2. Cormorants (
19 islands were used for terrestrial sampling; from these islands data about vegetation cover, aboveground plant biomass, plant species composition, arthropod densities and sampling design were available from former studies
In water, we randomly collected 6
All necessary permits were obtained from the county administrative board in Stockholm. Sampling on islands which are not protected areas need no permission according to Swedish law. The field studies did not involve endangered or protected species.
For P analyses in soil, samples with dominantly organic material were milled in a cychlotech mill to 0.5 mm, and sandy samples were homogenized in a machine mortar for maximum 3 minutes. Inorganic P was determined following extraction with 2% citric acid (1∶5 soil to extract solution)
Before analysis, the plant material was dried at 55°C to constant weight and all invertebrates were freeze-dried. Phosphorus content (%P, dry mass basis) was assayed using persulphate digestion and ascorbate-molybdate colorimetry
We compared soil N (NH4+ and NO3−) between the three groups of cormorant islands and reference islands with linear mixed effects models, using island category as fixed effect and island and sample depth as random effect. With ANOVA and Tukey post-hoc tests we compared N:C, P:C, and N:P mass ratios of terrestrial plants among the four island categories. We tested for differences in N:C, P:C, and N:P mass ratios between trophic groups (herbivores, detritivores, predators, and chironomids) with linear mixed effects models, using trophic group as fixed effect and island category, island and taxonomic group as random effect. We also compared N:C, P:C, and N:P mass ratios of 1) the three major terrestrial trophic groups (herbivores, detritivores, and predators) and chironomids and 2) the taxonomic arthropod groups between active and abandoned cormorant islands and reference islands with linear mixed effect models using island category as fixed effect and either 1) island, order and family, or 2) island as random effects. Similarly, we compared N:C, P:C and N:P mass ratios of algae (
We examined the relationship between consumer and resource stoichiometry by the homeostasis coefficient
We tested for effects of resource quality and quantity on terrestrial consumer densities with either multiple regressions or generalized linear models (glm) with a quasipoisson error structure depending on error distribution. Response variables were densities of arthropod groups, and explanatory variables were leaf NC-content, leaf PC-content and aboveground plant biomass (log-transformed). We chose the best model using the drop function in R and model comparison. To investigate if vegetation characteristics could also explain terrestrial arthropod densities we regressed densities against vegetation cover (sqrt-transformed) and plant species richness. Since these explanatory variable were correlated (t = 2.8, df = 15, p-value = 0.014, cor = 0.58) we tested their effects separately. We log-transformed arthropod densities if necessary in order to meet the assumption of normality and homoscedasticity. With linear mixed models we similarly investigated the relationship between resource quality and quantity and brackish invertebrate biomass (sqrt-transformed) using epiphytic algae N:C and P:C-ratios, epiphytic algae:
To investigate the relationship between consumer stoichiometry and consumer density/biomass response to cormorant nesting colonies we first calculated effect sizes among island categories for terrestrial (density) and brackish water (biomass) invertebrate groups. We compared the densities of the terrestrial taxonomic arthropod groups among three island categories (reference islands, abandoned and active cormorant islands) with ANOVA and Tukey post-hoc tests as described in Kolb et al. (2010)
Taxa | df,errordf | p | RF | AB | AC | E1 | df,errordf | p | CO | E2 | ||
Lepidoptera larvae | 2, 16 | 5.9±1.9 | 18.2±6.13 | 32.0±4.02 | 1.82 | 1, 17 | 27.9±3.8 | 1.63 | ||||
Auchenorrhyncha | 2, 16 | 0.2 | 0.861 | 45.1±17.4 | 60.3±30.6 | 50.7±14.3 | 0.22 | 1, 17 | 0.2 | 0.653 | 53.5±12.6 | 0.32 |
Aphidina | 2, 16 | 8.6±6.2 | 1.1±0.6 | 753±711 | 2.74 | 1, 17 | 528±499 | 1.68 | ||||
Curculionidae | 2, 16 | 8.1±2.4 | 35.4±7.0 | 3.3±1.4 | −1.13 | 1, 17 | 0.2 | 0.685 | 12.9±5.3 | −0.27 | ||
Chrysomelidae | 2, 16 | 24.0±11.4 | 29.0±14.93 | 16.6±2.7 | −1.2 | 1, 17 | 1.45 | 0.244 | 17.3±5.5 | −0.71 | ||
Isopoda | 2, 16 | 2.1 | 0.155 | 203.7±80 | 52.6±48 | 139.2±48.9 | −0.55 | 1, 17 | 1.9 | 0.188 | 113.2±38.0 | −1.03 |
Collembola | 2, 16 | 17.2±3.5 | 9.2±2.9 | 4.5±1.3 | −1.44 | 1, 17 | 5.9±1.4 | −1.16 | ||||
Brachycerid diptera | 2, 16 | 12±2.5 | 13.4±7.2 | 103.2±25.1 | 2.16 | 1, 17 | 76.3±22.1 | 1.41 | ||||
3, 15 | 2.6±1.1 | 2.3±1.8 | 38.0±17.4 |
1.54 | 3, 15 | |||||||
Araneidae | 2, 16 | 1.9 | 0.183 | 7. 4±1.7 | 25.6±9.1 | 11.7±4.8 | −0.22 | 1, 17 | 0.2 | 0.691 | 15.9±4.5 | 0.22 |
Linyphiidae | 2, 16 | 1.1 | 0. 343 | 18.1±6.0 | 44.2±25.5 | 20.6 4.1 | 0.27 | 1, 17 | 1.3 | 0.273 | 28.7±8.3 | 0.45 |
2, 16 | 1.0±0.7 | 6.8±1.8 | 2.3±0.9 | 1.59 | 1, 17 | 3.6±1.0 | 2.18 | |||||
2, 16 | 0.3 | 0.768 | 4.1±2.2 | 9.6±5.5 | 4.8±3.6 | 0.06 | 1, 17 | 0.1 | 0.734 | 6.3±2.9 | 0.41 | |
Lycosidae | 2, 16 | 19.8±4.5 | 22.8±5.9 | 02.8±1.6 | −2.1 | 1, 17 | 8.8±3.6 | −1.37 | ||||
Parasitic hymenoptera | 2, 16 | 4.8±0.9 | 6.9±3.2 | 10±1.0 | 0.90 | 1, 17 | 9.4±1.2 | 0.66 | ||||
Coccinellidae | 2, 16 | 2.9±0.6 | 3.7±1.5 | 12.3±0.42 | 1.43 | 1, 17 | 9.7±2.3 | 1.1 | ||||
Carabidae | 2, 16 | 1.54±0.32 | 2.44±0.65 | 0.73±2.7 | −0.81 | 1, 17 | 0.3 | 0.578 | 6.0±2.3 | −0.29 | ||
Staphylinidae | 2, 16 | 0.9 | 0.416 | 4.1±1.4 | 7.3±2.0 | 5.8±2.0 | 0.45 | 1, 17 | 1.3 | 0.265 | 6.3±1.5 | 0.64 |
Nabidae | 2, 16 | 0.7 | 0.524 | 1.3±0.5 | 4.7±4.2 | 5.1±2.9 | 0.68 | 1, 17 | 1.4 | 0.259 | 5.0±2.3 | 0.62 |
Formicidae | 2, 16 | 0.4 | 0.670 | 71.3±31.1 | 88.2±46.1 | 50.9±21.6 | −0.19 | 1, 17 | 0.0 | 0.976 | 62.1±19.8 | −0.01 |
For Chironomidae E2 = E1.
Shown are df, error df, F- and p- values, mean (±SE) individual numbers per island and effect size (E1 and E2). Significant (p>0.05) differences are bold in the table, marginal significant differences (p = 0.051–0.099) are cursive and bold.
Effect sizes for brackish invertebrates (E1brack) were calculated based on the difference in biomass (mean ± SE) between reference islands and the active cormorant islands with high nest density from linear mixed effect models in Kolb et al. (2010)
We tested for a relationship between consumer elemental mass ratios (N:C and P:C) and the effect size on consumer response with a regression analysis. Since soil and plant N-contents were only increased on active cormorant islands we regressed E1terr and the consumer N:C mass ratios. Soil and plant P contents were increased on both abandoned and active cormorant islands, therefore we regressed E2terr and the consumer P:C mass ratios. Finally, algal nutrient content (both N and P) was only increased around active cormorant islands with high nest densities and we regressed E1brack with both consumer N:C and P:C mass ratios. We repeated the analysis with consumer nutrient limitation (L) as independent variable. Nutrient limitation (L) was defined as elemental mismatch between consumer and its resource on reference islands.
All statistical tests were performed in the free software R 2.10.0 or 2.12.1.
Plant available N (NH4+ and NO3−) (mg/100 g dry soil) was 15-fold higher on islands with low cormorant nest density and 9-fold higher on islands with high nest density than on reference islands and about equal on abandoned and reference islands (F = 7.2, p = 0.021, dendf = 6, n = 50;
Different letters indicate significant differences in linear mixed effect model (A and B) and post-hoc test (C–E).
Terrestrial plants generally had higher N:C and P:C mass ratios on active cormorant islands than on reference islands (
The horizontal range corresponds to the range of the soil N and P. The grey diagonal line represents the 1∶1 relation. See
Algae, generally, had smaller differences in elemental composition between island categories than terrestrial plants (
Different letters indicate significant differences in linear mixed effect model.
The analysis of elemental mass ratios for terrestrial and brackish invertebrates revealed a wide variation among taxa and only small variations, for a few taxa, between island categories.
The N:C mass ratios showed a 2-fold difference among terrestrial arthropods, collembolans had the highest and aphids the lowest N:C mass ratio (
Solid lines indicate herbivores, dashed lines detritivores, and dotted lines predators. The horizontal range corresponds to the data range of the resource. The grey diagonal line represents the 1∶1 relation.
The N:C mass ratios of all terrestrial trophic groups were about equal among island categories (
Taxa | N:C | P:C | N:P | |||||||||
n | is | n | is | N | is | |||||||
141 | 15 | 0.3 | 0.78 | 53 | 16 | 1.2 | 0.34 | 53 | 16 | 0.2 | 0.83 | |
Aphidina | 7 | 5 | 2.3 | 0.31 | ||||||||
Cercopidea | 45 | 14 | 1.0 | 0.39 | 13 | 13 | 3.4 | 0.08 | ||||
Lepidoptera larvae | 41 | 15 | 0.4 | 0.74 | 15 | 15 | 1.0 | 0.39 | 15 | 15 | 1.0 | 0.39 |
Chrysomelidae | 25 | 16 | 0.1 | 0.89 | 14 | 14 | 0.0 | 0.97 | 14 | 14 | 1.2 | 0.33 |
Curculionidae | 11 | 11 | 1.7 | 0.24 | 11 | 11 | 0.4 | 0.69 | ||||
84 | 15 | 0.1 | 0.88 | 14 | 14 | 0.9 | 0.45 | 14 | 14 | 1.2 | 0.36 | |
Isopoda | 70 | 15 | 0.3 | 0.72 | 14 | 14 | 0.9 | 0.45 | 14 | 14 | 1.2 | 0.36 |
Collembola | 14 | 10 | 4.4 | 0.06 | ||||||||
Brachycerid diptera | 32 | 11 | 13 | 0.32 | ||||||||
51 | 15 | 3.6 | 0.06 | 13 | 13 | 1.3 | 0.31 | 13 | 13 | 0.1 | 0.92 | |
445 | 20 | 1.4 | 0.28 | 40 | 14 | 0.4 | 0.69 | 41 | 15 | 0.1 | 0.88 | |
Araneidae | 65 | 16 | 0.4 | 0.69 | 13 | 13 | 0.3 | 0.75 | 13 | 13 | 0.2 | 0.86 |
Linyphiidae | 10 | 10 | 0.2 | 0.81 | 10 | 10 | 1.4 | 0.31 | ||||
Tetragnathidae | 57 | 11 | 0.0 | 1.0 | ||||||||
Lycosidae | 55 | 11 | 4.3 | 0.05 | ||||||||
Coccinellidae | 34 | 14 | 1.0 | 0.41 | 12 | 12 | 0.0 | 0.97 | 12 | 12 | 0.4 | 0.68 |
Carabidae | 53 | 16 | 1.3 | 0.31 | 6 | 6 | 0.2 | 0.81 | 6 | 6 | 0.3 | 0.73 |
Staphylinidae | 23 | 9 | 1.7 | 0.27 | ||||||||
36 | 9 | 0.3 | 0.74 | |||||||||
Formicidae | 58 | 13 | 1.0 | 0.40 |
Shown are the number of samples (n), number of islands (islands), F- and p- values from ANOVA for lme. Significant (p>0.05) differences are bold in the table.
The N:C mass ratios of brackish invertebrate differ only slightly for
n | is | F | p | Slope | Mean± SE | |
(mean ± SE) | ||||||
91 | 17 | |||||
Island category (df = 3) | 1.4 | 0.278 | 0.182±0.002 | |||
Wave exposure (df = 1) | 7.0 | 0.010 | −0.009±0.003 | |||
Theodoxus fluviatilis | 76 | 15 | ||||
Island category (df = 3) | 1.2 | 0.368 | 0.221±0.003 | |||
121 | 17 | |||||
Island category (df = 3) | 1.8 | 0.204 | 0.186±0.003 | |||
142 | 17 | |||||
Island category (df = 3) | 1.9 | 0.177 | 0.161±0.002 | |||
66 | 15 | |||||
Island category (df = 3) | 4.7 | 0.025 | 0.151±0.003 | |||
Wave exposure (df = 1) | 0.1 | 0.708 | ||||
Island×Wave (df = 3) | 17.8 | <0.0001 | ||||
26 | 14 | 0.014±0.001 | ||||
Island category (df = 3) | 1.9 | 0.201 | ||||
34 | 17 | |||||
Island category (df = 3) | 0.7 | 0.578 | 0.041±0.002 | |||
30 | 15 | |||||
Island category (df = 3) | 2.2 | 0.145 | 0.028±0.001 | |||
26 | 14 | |||||
Island category (df = 3) | 2.6 | 0.112 | 13.67±0.83 | |||
34 | 17 | |||||
Island category (df = 3) | 1.0 | 0.439 | 4.99±0.37 | |||
30 | 15 | |||||
Island category (df = 3) | i | 1.4 | 0.297 | 6.47±0.39 |
Shown are the number of samples (n), number of islands (islands), F- and p- values from ANOVA for lme, the slope for wave exposure, and mean ± SE over all islands. Significant effects in bold (p<0.05).
The P:C mass ratios among terrestrial arthropods showed a 4.4-fold difference; isopods had the highest and beetles had the lowest P:C (
The P:C mass ratios of all terrestrial and brackish trophic groups were about equal among island categories, and only two taxonomic groups (Cercopidae and
N:P mass ratios differed between detritivores (isopods) and the other trophic groups (F = 13.3, p<0.0001, den df = 102, n = 121) (
Among invertebrate groups 17 out of 25 showed differences in density or biomass among island categories (
When testing plant quality or quantity effects we found that the densities of 6 taxonomic arthropod groups (Aphidina, brachycerid Diptera, Chironomidae, Coccinellidae, and parasitic Hymenoptera) were positively and 5 groups (Chrysomelidae, Curculionidae, Collembola, Carabidae, and Lycosidae) were negatively correlated with leaf NC-content (
Taxa | mo | Leaf NC-content | Leaf PC-content | Plant biomass | |
Aphidina | lm | (+) | F = 7.4, p = 0.017, | ||
df = 14, R2 = 29.8% | |||||
Cercopidea | glm | (+) | P(χ2) 0.015 | ||
df = 14 | |||||
Lepidoptera larvae | lm | (+) | F = 33.0, p<0.0001 | ||
df = 13, R2 = 69.6% | |||||
Chrysomelidae | lm | (−) | (+) | ||
t = −6.3, p<0.0001 | t = 4.6, p<0.001 | ||||
Curculionidae | glm | (−) | (+) | ||
t = −3.5, p = 0.004, | t = 3.1, p = 0.008 | ||||
P(χ2) = 0.001, df = 14 | P(χ2) 0.002, df = 13 | ||||
Herbivorous Heteroptera | lm | ||||
lm | |||||
Isopoda | lm | ||||
Collembola | lm | (−) | (−) | F = 16.1, p<0.001, | |
t = −3.6, p<0.003 | t = −2.5, p<0.026 | df = 13, R2 = 66.8% | |||
Brachycerid | lm | (+) | F = 28.8, p<0.001, | ||
Diptera | df = 14, R2 = 62.3% | ||||
lm | (+) | F = 10.0, p<0.006, | |||
df = 14, R2 = 37.6% | |||||
Araneidae | lm | ||||
Linyphiidae | lm | ||||
Tetragnathidae | glm | (+) | |||
t = 2.7,p = 0.016, | |||||
P(χ2) <0.002, df = 14 | |||||
Pachygnatha | lm | ||||
Lycosidae | glm | (−) | |||
t = −2.8,p = 0.015, | |||||
P(χ2) <0.002, df = 14 | |||||
Coccinellidae | glm | (+) | (+) | ||
t = 6.2, p<0.0001 | t = 4.7, p<0.001 | ||||
P(χ2) <0.0001, df = 14 | P(χ2) <0.0001, df = 13 | ||||
Carabidae | lm | (−) | (+) | F = 14.2, p<0.001, | |
t = −3.9, p = 0.002 | t = 3.3, p = 0.005 | df = 13, R2 = 63.8% | |||
Staphylinidae | lm | ||||
Nabis spp. | glm | ||||
Formicidae | lm | ||||
Parasitic | lm | (+) | F = 18.5, p<0.001, | ||
hymenoptera | df = 14, R2 = 53.8% |
Shown are the direction of effect positive (+) and negative (−). Only significant results are shown (p>0.05).
n | is | Slope | |||
(mean ± SE) | |||||
Epi:Fu-ratio | 99 | 17 | 17.1 | 0.0001 | 0.86±0.21 |
Theodoxus fluviatilis | |||||
Epi:Fu-ratio | 99 | 17 | 0.8 | 0.361 | 0.83±0.90 |
Wave exposure | 99 | 17 | 23.3 | <0.0001 | −1.82±0.38 |
Epi:Fu-ratio * Wave exposure | 99 | 17 | 8.3 | 0.005 | 2.25±0.78 |
Algal P:C-content | 34 | 16 | 7.9 | 0.013 | 545±194 |
Wave exposure | 99 | 17 | 4.4 | 0.040 | −0.67±0.32 |
Epi:Fu-ratio | 99 | 17 | 0.2 | 0.640 | 0.17±0.41 |
Wave exposure | 99 | 17 | 5.7 | 0.019 | −0.35±0.14 |
Epi:Fu-ratio * Wave exposure | 99 | 17 | 6.6 | 0.012 | 0.91±0.35 |
Wave exposure | 99 | 17 | 18.0 | 0.0001 | −0.15±0.04 |
Shown are the number of samples (n), number of islands (islands), F- and p- values from ANOVA for lme. Significant effects in bold (p<0.05). Algal N:C-content did not have any significant effect and is therefore not shown in the table.
Among other vegetation variables, vegetation cover correlated with the density of the same arthropod groups as leaf N:C-ratios (expect Coccinellidae), but inversely. Plant species richness correlated positively with the density of Collembola and Lycosidae and negatively with the density of brachycerid Diptera and Chironomidae (
We found that nesting cormorants radically changed soil nutrient composition, plant nutrient content and assumingly resource quality to herbivores and detritivores. In contrast, invertebrates generally had only small differences in either N:C or P:C mass ratios between island categories. On reference islands, there was a large difference in N and P content between plants and plant consumers (terrestrial and aquatic herbivores and detritivores) similar to previous studies
The differences in soil and plant nutrient content among island categories and between land and water suggest that the fate of N and P in cormorant guano depend on cormorant density and colonization history. As expected, islands with active nesting by cormorants generally had much higher soil N and P contents than reference islands, and plant N content increased with an increasing cormorant density. On abandoned islands, however, soil N content was similar to reference islands whereas soil P content was similar to active nesting islands, and this change was also reflected in the P:C and N:C mass ratios of plants. At the same time, plant biomass tended to be higher on abandoned than on reference islands
In contrast to plant nutrient content, invertebrates had only small differences in N:C or P:C mass ratios between island categories. To estimate these ratios, we pooled samples of related species and the small differences can therefore not be directly interpreted as elemental homeostasis. The mean nutrient content in invertebrates could also be affected by changes in species composition among islands with and without cormorant nesting colonies. Kolb et al. (2012)
Irrespective of the cause for the apparent homeostasis of invertebrate herbivores and detritivores, we can conclude that for the next trophic level, predators or parasitoids, there is no obvious change in diet quality between island categories in this study. Thus, we found no evidence for the hypothesis that cascading bottom-up effects may be mediated by qualitative changes in primary consumers
A previous study in Neotropical streams found, in contrast to our study, that most taxonomic invertebrates groups in chronic P enriched Neotropical streams had two-fold higher P content than invertebrates in low-P streams
Using data from two parallel studies
When further investigating effects of plant quality (leaf/algae NC and PC-content) and quantity (aboveground plant biomass/epiphytic algae:
Several taxonomic groups had surprisingly a negative density response to leaf N:C-content. The literature contains few examples where arthropod densities or fitness decrease at a high resource nitrogen content
The limited evidence that N and P content was a prime determinant of invertebrate density or biomass in our system does not imply that arthropods in our system are not nutrient limited but rather that other factors are more important determinants of population growth. The connection between N and P contents and population growth rates may be weak because other factors are more important determinants of population growth. For instance, P contents among terrestrial invertebrate species seem to be best predicted by variation in body size
To conclude, our study indicates that ecological stoichiometry seem less able to predict arthropod responses to variation along a resource gradient. It is unclear whether this limited predictability is due to that other factors than nutrient content are more important in our complex system, or that the conditions for understanding nutrient limitation is different in terrestrial arthropods than planktonic crustaceans.
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We gratefully acknowledge L and S Jerling, A Lindström, C Essenberg and A Sjösten for assistance in the field and in the lab.