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Stickleback diets in bays along the northern Baltic sea
Douglas Skarp
Student
Degree Thesis in Biology 15 ECTS Bachelor’s level
Report passed 2019-06-05 Supervisor: Pär Byström
Abstract
Coastal populations of perch (Perca fluviatilis) in the Baltic Sea has declined substantially the last decades while the populations of three-spined sticklebacks (Gasterosteus
aculeatus) has increased rapidly during the same time period. Earlier studies have suggested that predation on perch larvae and or competition from sticklebacks are the causes behind the decline in perch. To test if predation from sticklebacks commonly occur on perch larvae as well as provide data on stickleback diets in general, diets of
sticklebacks were examined by looking at the stomach content of collected samples of sticklebacks from different bays along the Swedish and Finnish coast. Results showed no evidence of stickleback predation on perch larvae as no perch larvae were found in any of the examined stomachs. Three-spined sticklebacks generally had the same diet in all studied bays consisting mainly of Chironomidae and Asellus aquaticus. The diet results suggest that competition between perch larvae and sticklebacks is minor if any due to low proportions of zooplankton found in the stomachs of the sticklebacks while zooplankton is the main food source for perch larvae. In bays where three spined sticklebacks were found with nine-spined sticklebacks they generally had similar diets. Still, due to a larger size and gape size of three-spined sticklebacks they fed more on larger prey like Asellus aquaticus while nine-spined sticklebacks contained smaller prey such as benthic
cladocerans. Due to few samples from bays where sticklebacks were found together with perch larvae, no conclusion regarding predation on larvae as the main the mechanism for declines in coastal perch population can be drawn from the results in this study.
Table of contents
1 Introduction………1
1.1 Background………..………... 1
1.2 Aim………..………. 1
2 Materials and methods……….….…..2
2.1 Collection and stomach examination………..….. 2
2.2 Measuring gape size of three-spined and nine-spined Sticklebacks……… 3
2.3 Statistical analysis……… 3
3 Results………4
4 Discussion………6
4.1 Implication of the results………. 6
4.2 Conclusion………...…… 8
5 Acknowledgements……….8
6 References………..8
1 Introduction
1.1 Background
Since the last ice age the parts of the world then covered in ice have, and is still,
experiencing raising of the landmass over the sea in form of post glacial isostatic rebound (Fjeldskaar et al. 2000). This rebound has led, and is still leading, to the formation of new shallow bays along the coast (Strahler and Strahler 2005).
It has been observed that the populations of three-spined sticklebacks (Gasterosteus aculeatus) have increased substantially since 2002 (Eriksson et al. 2009), while local populations of perch (Perca fluviatilis) in parts of the Bothnian sea have declined substantially (Ljunggren et al. 2010) in these habitats. This dramatic decrease cannot be considered to be general along the Baltic coast as increases in catch of perch have been observed in other parts of the Baltic Sea during the same timeframe (Ådjers et al. 2006).
The increase in sticklebacks can in part be contributed to the selective targeting of fisheries of larger predatory fish like cod, leading to a predation release and a rapid increase in abundance of their smaller prey fish such as sticklebacks (Eriksson et al.
2011). Other sources point towards regime shifts as a result of human-induced
eutrophication of the Baltic sea to have a leading role in the depletion of large predatory fish due to lower oxygen and salinity levels in the deep basins where they spawn
(Österblom et al. 2007; Larsson, Elmgren, and Wulff 1985). Sticklebacks, who migrate into coastal areas from the offshore areas of the Baltic sea in order to reproduce, have been observed to have a negative impact on the recruitment of young perch when they both spawn in the same bays (Byström et al. 2015). Though the main mechanism behind the decreased recruitment of perch has been found to be towards predation by
sticklebacks on perch larvae by some sources (Fauchald 2010; Byström et al. 2015), it has also been suggested to be partly due to competition for zooplankton with sticklebacks (Ljunggren et al. 2010; Bergström et al. 2015). This competition arises from a certain stage in the life history of the perch. During their growth, perch undergo three
ontogenetic shifts in diet to correspond with their size, first eating zooplankton, going on to macroinvertebrates, and finally becoming piscivorous at larger sizes (Persson and Greenberg, 1990).
According to all these mechanisms, a large population of larger predatory fish (perch) will secure successful recruitment of their own young through predation on and control of the populations of prey fish (sticklebacks) (Byström et a 2015). In contrast, a large population of prey fish predating on young predatory fish will reduce their success of recruitment and increase their own populations by doing so (Fauchald 2010, Byström et al, 2015). Studies have shown that complex ecosystems, like the one in the Baltic Sea, can exhibit more than one stable state and experience abrupt regime shifts between these states (Sheffer et al.
2001). Changes to an ecosystem can at first seemingly have little effect until a threshold is reached, abruptly changing the regimes (Sheffer and Carpenter 2003). These alternative states are upheld by feedback mechanisms and can therefore be difficult to reverse (Sheffer et al. 2001; Sheffer and Carpenter 2003).
1.2 Aim
The aims of this study were to A) investigate whether predation of three-spined
sticklebacks on perch larvae is common in shallow bays used by both species for spawning by analyzing the stomach content of sticklebacks. B) to study the diets of three-spine sticklebacks in general to obtain information on potential competitive interactions with young of the year (YOY) perch, but also with nine spine sticklebacks (Pungitius
pungitius). Alongside the above, the diets of nine-spined sticklebacks was also studied in
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bays when found together with three-spined sticklebacks in order to identify potential competitive interactions and niche overlaps between the two species.
2 Materials and methods
2.1 Collection and stomach examination
During the summer of 2018 sticklebacks and YOY of perch were quantified in a large number of shallow bays along the coasts of northern Baltic Sea in both Västerbotten, Sweden, and Österbotten, Finland in the EU financed project Kvarken Flada. The sticklebacks and perch were sampled from creels put in the bays overnight, and thesamples were placed in ethanol for preservation. The sampled YOY perch were counted and individually measured for length. From data collected at the sampled locations four categories of stickleback populations (bays) were examined and contrasted to each other. The original aim was to use 30 individuals from 4 replicates (different bays) per category, but due to lower number of individuals found in some bays this was not always possible. Because of this lack of usable samples for the study, the same bays were assigned for
more than one group of sticklebacks. In the cases where this was done, the different categories of sticklebacks from the same bays were collected at different times, at least two weeks apart. The same bay was not used more than once for each category.
Table 1. Description of bays used in the study. The first column shows the bay types. The second column shows the map ID of each bay, the name, the date it was sampled, and an assigned number. The third column shows how many individuals were sampled from each location with their mean size and standard deviation. A maximum amount of 30 individuals per category up to 4 replicates was always used if possible.
Note that three of the bays (Klösviken, Ö. Stadsviken, and Laxögern) were sampled two times and used in two bay categories but given different numbers for simplicity.
Location description and category number
Map ID, location name, date of sampling, and bay
number
Number of individuals sampled per location and their mean size in cm Category 1 (a) Bådafjärden 18-06-06 (Bay 1) 30 (6.35 ± 0.31)
Fig. 1. Sampling sites of sticklebacks and perch larvae along the northern Baltic Sea. See Table 1. for names.
4 locations of three-spined sticklebacks found without the presence of YOY perch (Bays 1-4)
(k) Träskholmsfjärden 18-06-05 (Bay 2)
(h) Bredviken 18-05-13 (Bay 3) (f) Klösviken 18-06-06 (Bay 4)
30 (6.32 ±0.39)
30 (6.11 ± 0.56) 30 (6.21 ± 0.39) Category 2
2 locations of three-spined sticklebacks found together with a high abundance of YOY perch (Bays 5-6)
(j) Godhamnen 18-05-23 (Bay 5) (f) Laxögern 18-05-23 (Bay 6)
9 (6.46 ± 0.24) 7 (6.29 ± 0.25)
Category 3
4 locations of three-spined sticklebacks found without the presence of YOY perch. YOY perch had been observed earlier during the season (Bays 7-10)
(g) Ö. Stadsviken 18-05-23 (Bay 7)
(b) Bukten 18-05-30 (Bay 8) (e) Laxögern 18-06-07 (Bay 9) (c) S. Grundfjärden 18-06-13 (Bay 10)
30 (6.09 ± 0.31)
30 (6.28 ± 0.32) 30 (6.21 ± 1.26) 24 (6.18 ± 0.28)
Category 4
4 locations of three-spined and nine-spined sticklebacks found together, without YOY perch (Bays 11-14)
(f) Klösviken 18-06-24 (Bay 11)
(g) Ö. Stadsviken 18-06-06 (Bay 12)
(d) Långviken 18-06-08 (Bay 13) (i) Bysund 18-05-25 (Bay 14)
Three- and nine-spined 30 (6.36 ± 0.25) - 30 (4.93 ± 0.82)
30 (6.34 ± 0.33) - 30 (5.00 ± 0.35)
9 (6.11 ± 0.51) - 30 (4.62 ± 0.41) 30 (6.38 ± 0.24) - 30 (4.57 ± 0.52)
In a laboratory all sticklebacks were measured to the nearest 0.1 cm, and stomach and intestine of the individuals were removed and placed under a stereoscope. The stomach was cut open and the contents were moved to a petri dish with ethanol. All stomach contents were identified taxonomically as far as possible, measured, and counted.
2.2 Measuring gape size of three-spined and nine-spined sticklebacks
The gape size of both three-spined and nine-spined sticklebacks were measured in order to test for differences in gape limitation between the two species and create a length-gap size regression. 30 individuals from each species was measured, with three additional larger specimens of nine-spined sticklebacks from a freshwater pond to see if potential trends would continue. The fish was placed under a stereoscope and a plastic cone with an angle of 30° was inserted into its mouth. When the upper and lower jaw formed a 90°angle the size of the gape height was measured to the nearest 0.1 mm.
2.3 Statistical analysis
Length – dry weight regressions for different groups of organisms were used to calculate the biomass of each taxa in each stomach (Bagenal 1971; Edwards et al. 2009; Giustini et al. 2008; Johansson 1992; Castilho-Noll and Arcifa, 2007; Dumont et al. 1975; Bottrell et al. 1976; Persson and Greenberg 1990; Berg 2000). After the biomass of the stomachs’
contents had been estimated, they were added up and divided into nine prey categories:
Chironomidae (consisting of both larvae and pupae), Asellus aquaticus, Macrocrustacea (consisting of Gammarus och Mysida), Benthic cladocerans, Copepoda (consisting of all species of copepods), Corixa, EPTA (consisting of larvae of Ephemeroptera, Plecoptera, Trichoptera, and Anisoptera), Fish eggs (consisting of eggs of sticklebacks), and Other (small quantities of Acari, Hirudinea, Tipulidae, and larvae and adults of Coleoptera).
These categories were then compared through a series of t-tests between the populations of the nine-spined and the three-spined sticklebacks found together in order to test for
4 4
differences in diets between the two species. As all data was gathered per individual, a non-metric multidimensional scaling (nMDS) analysis was also used to show
dissimilarities (or similarities) in diet composition for each individual of three-spined and nine-spined sticklebacks in the bays where they coexisted. From the proportion data, a Bray–Curtis dissimilarity matrix was calculated using the function metaMDS from vegan R package (Oksanen et al. 2016). One-way ANOVA tests were run for the three large groups of three-spined sticklebacks to test for differences in diets between the different defined bay categories.
3 Results
From the 469 stickleback stomachs examined, none showed any sign of containing larvae of perch, or any residue of it or of other fish apart from stickleback eggs (Fig 2a).
The diets of three-spined sticklebacks showed no evident differences between the different bays and overall diets were similar in all bays (Fig 2a). ANOVA tests of differences between bay categories 1, 3, and 4 (Table 1) showed only a statistical
difference for Asellus aquaticus (One-way ANOVA, F=8.01, FCritical=4.26, P<0.01) all other prey categories non-significant (One-way ANOVA, F=0.83–4.17, P=0.052–0.468).
Asellus aquaticus was consumed to larger extent in bays 6, 7, 8, and 14, and to smaller
Fig. 2. The proportions of the prey found in the stomachs of all sticklebacks examined, portrayed by the bay they were sampled from. The number of the bays from a corresponds with the number from b.
0%
20%
40%
60%
80%
100%
1 2 3 4 5 6 7 8 9 10 11 12 13 14
Chironomidae Asellus Macrocrustacea Benthic cladocerans Copepods Corixa
EPT+Anisoptera Fish eggs Other
0%
10%
20%
30%
40%
50%
60%
70%
80%
90%
100%
1 2 3 4 5 6 7 8 9 10 11 12 13 14
Chironomidae Asellus Macrocrustacea Benthic cladocerans Copepods Corixa
EPT+Anisoptera Fish eggs Other b
a
extent in bays 5, 10, 11 and 12 (Fig 2a). Other bays showed low to no proportions of Asellus aquaticus in stomachs.
Pairwise t-tests were run on all prey categories comparing three-spined to nine-spined sticklebacks’ diets from bay category 4. The only t-test that showed a significant difference was benthic cladocerans, of which nine-spined sticklebacks consumed more than the three-spined sticklebacks (t3=-2.89, P=0.03), all other prey categories non- significant (t3=-1.30–1.83, P=0.08–0.49) (Fig 2a,b).
The gape-sizes of nine-spined sticklebacks and three-spined
sticklebacks both showed a monotonic increase with fish length (Fig. 3). For three-spine sticklebacks the measured gape size - body size relationship was similar to previous measurement by Byström et al. (2015). The
relationships show that nine-spined sticklebacks have a smaller gape size for the same body length than a three- spined sticklebacks but only at larger sizes (Fig. 3). The linear relationship for the three-spined stickleback is steeper than that of the nine-spined, showing that they will have a
relatively larger gape size with increased body length compared to nine-spined sticklebacks.
y = 0,0651x - 0,5708 R² = 0,8965
y = 0,0764x - 0,7088 R² = 0,8395
y = 0,01x1,4569
1 1,5 2 2,5 3 3,5 4 4,5 5 5,5
25 35 45 55 65 75
Gape size 90°angle (mm)
Stickleback length (mm)
Stickleback Gape Size
Fig. 3. The relationship between gape size and body length of three-spined (pink) and nine-spined
sticklebacks (blue). The dotted line for each species represents the predicted gape size for a given length. The transparent black line together with the middle equation shows data from previous studies of three-spined stickleback gape size as a reference (Byström et al. 2015). The yellow sample represents a small sample nine- spined sticklebacks from a small freshwater pond used as control to test if the trend for smaller gape size of nine-spined sticklebacks holds at larger sizes.
0%
5%
10%
15%
20%
25%
30%
6 7 8 9 10 11 12 13 14 15 Proportion of Asellus sizes
Size (mm)
Three-spined Stickleback
0%
5%
10%
15%
20%
25%
30%
6 7 8 9 10 11 12 13 14 15 Proportion of Asellus sizes
Size (mm)
Nine-spined Stickleback
a
b
Fig. 4. The size distribution (proportion) of Asellus in diets of a) three-spined and b) nine-spined sticklebacks in bays where they coexisted. Total number of Asellus found in stomachs for three-spined sticklebacks were 18 and for nine-spined sticklebacks 20.
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6 The size of consumed Asellus
aquaticus (Fig. 4 a,b) shows a tendency to be larger for three- spined sticklebacks, with larger maximum size consumed but mean size consumed did not differ significantly (t-test t3=0.03,
P=0.49).
Still, overall the stomachs of three-spined sticklebacks seem to include larger prey than nine- spined sticklebacks (Fig. 5). More three-spined than nine-spined sticklebacks were associated with larger prey categories like three- spined stickleback eggs and macro crustaceans, while most nine- spined sticklebacks were associated with smaller prey categories like Chironomidae, others (only Acari was found in the stomachs of nine-spined sticklebacks) and cyclopoid
copepods when found in the same bays. It does however further suggest that the availability of food differs between bays.
Data from the count board sampling of the bays showed a tendency of the number of YOY perch to decrease over the summer, while three-spined stickleback was shown to increase in numbers during the same time (results not shown). Trends generally followed that of Laxögern where sampling 2018-05-25 yielded 515 perch larvae and 17 three-spined sticklebacks, and sampling 2018-06-07 yielded no perch larvae and 69 three-spined sticklebacks.
4 Discussion
4.1 Implications of the results
As stated in the results, no remains of perch larvae were found in the diets of three-spined sticklebacks. Nothing could be found even in the two bays at the time when perch larvae were abundant and coincided with low densities of sticklebacks. Contrary to the original plan, high densities of three-spined sticklebacks could not be found together with YOY perch in the bays sampled, which still in a way is not entirely surprising considering that declines in perch have been shown to coincide with increasing densities of sticklebacks in coastal areas during the last decades (Ljunggren et al. 2010, Bergström et al. 2015, Byström et al. 2015). Interestingly, and in line with both Byström et al. (2015) and Bergström et al. (2015), at the second occasion of sampling in one of the bays (Laxögern) with high densities of perch larvae, no larvae were found and stickleback densities had increased dramatically. Byström et al (2015) have suggest that this decline is mainly due to stickleback predation, while others have suggested that competition for zooplankton is the main cause of declines in perch larvae at high densities of sticklebacks (Ljunggren et
Fig. 4. The size distribution (proportion) of Asellus in diets of a) three-spined and b) nine-spined sticklebacks in bays where they coexisted. Total number of Asellus found in stomachs for three-spined sticklebacks were 18 and for nine-spined sticklebacks 20.
Fig. 5. nMDS analysis of the proportion of prey analyzed individually for each specimen from the bays where three-spined and nine-spined sticklebacks were found together. 9ss represents nine-spined sticklebacks and 3ss represents three-spined sticklebacks. The different colors represent the different bays the sticklebacks were collected.
al. 2010; Bergström et al. 2015). The results showing that three-spined sticklebacks’ diets were to a very small extent made up by zooplankton, the only food source that perch larvae feed on (Byström et al. 1998), suggesting that competition from sticklebacks is not the main cause of the for the disappearance of perch larvae in that bay. Although in this instance no larvae were found in the stomachs of sticklebacks it may well be due to the fact that fish larvae do not last long in the stomachs of predatory fish (Moodie 1972) and the fish being stuck for a time in the traps before being put in ethanol. I can therefore not rule out predation from sticklebacks to be the main cause of the decline between the two sampling dates in Laxögern as experimental evidence and field data suggest strong predation rate on perch larvae by sticklebacks (Byström et al. 2015). In the three other bays where perch larvae had been found earlier in the season, the larvae could also have been consumed long before the sticklebacks for this analysis were sampled.
The proportions of the contents found in the stomachs of the sticklebacks mainly consisted of benthic insects and larvae. This was true for all bays examined, both on the Swedish and Finnish side. Chironomidae dominated the diets of both three-spined and nine-spined sticklebacks in most bays, while Asellus aquaticus and EPTA dominated others. Smaller prey than Chironomidae like zooplankton, while sometimes abundant in number, never made up a large proportion of the biomass found in the stomachs.
Considering that zooplankton is the only prey perch larvae feed on (Byström et al. 1998), competition between sticklebacks and perch larvae seems unlikely to be a leading cause of the decline of perch.
The statistical tests showed no differences or only minor differences in the diet of the three-spined sticklebacks regarding if they were sampled from bays when they were alone or where either YOY perch or nine-spined sticklebacks had been found. Considering the apparent differences in diet and size of prey, competition might not be strong between the species. Benthic cladocerans were the only prey category shown to have a statistical significance when comparing three-spined and nine-spined sticklebacks (t3=-2.89, P=0.03). Because no statistical difference could be found in the stomach contents for any other prey category comparing the three-spined and nine-spined sticklebacks, the results indicate that both species feed on these prey and might compete over them. Considering the other data gathered by this study, the truth might not be as simple as that due to the t- tests not factoring in prey size and gape limitations. Even though the species might seem to compete with each other (Fauchald 2010; Byström et al. 2015), the competition might not be as intense and their niches might not be as overlapping as first thought due to different preferences in habitats and foraging strategies (Hart 2003). Nevertheless, this study contributes to the scare knowledge of the early summer diets of both three and nine-spine sticklebacks in coastal bays in the Baltic sea.
While an overlap can be found in prey size, the data would suggest the nine-spined sticklebacks to be somewhat limited by their gape sizes due to larger prey not being found in any of their stomachs while abundant in stomachs from three-spined sticklebacks from the same bay. The gape size to body size relationship was shown to differ slightly between nine-spined and three-spined sticklebacks, though the main difference was purely that of body size. However, a steeper linear relationship for the three-spined than the nine- spined sticklebacks would suggest larger possible gape size with increased length for three-spined. Taking this into consideration, the nine-spined sticklebacks in this study due to their smaller body size appear to be more constrained by their gape size and therefore feed on smaller prey compared to three-spined sticklebacks. Hence, three- spined sticklebacks diets consisted more of stickleback eggs and larger macrocrustaceans, whereas the nine-spined instead relied on smaller prey like Chironomidae. This may indicate that the different species of stickleback are not competing strongly with each
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other even though a considerable part of their diets for the two species was similar when coexisting in the same bays. This is in line with previous observations showing that they appear to mostly have the same diets (Hynes 1950). Still, the difference found in this study may part from the obvious size difference also relate to that the two species have been shown to use different microhabitats and utilize differing foraging methods even when found together (Hart 2003).
4.2 Conclusion
In conclusion, my results cannot themselves rule out that stickleback predation on YOY perch is the main reason for their decline. Competition between sticklebacks and perch larvae seems to be an unlikely reason for it according to the results of the study. If we do not consider anthropogenic effects on populations, predation by sticklebacks still seems most likely to be the main cause of the decline of perch as it has previously been shown to be strong. This would be true for most shallow bays along Bottenviken due to the
sticklebacks sampled from both the Swedish and Finnish side having very similar diets.
The differences in gape sizes would explain the differences in prey consumed by the two stickleback species. While the three-spined stickleback in general ate more larger prey like Asellus aquaticus and nine-spined stickleback ate smaller ones like benthic cladocerans, their diets did not differ considerably in terms of taxa eaten. Keeping the different choices of microhabitats and foraging methods in mind together with the gape sizes, the
competition between the species might not be as intense as first hypothesized even though their diets seem similar.
5 Acknowledgements
This study was made possible by Länsstyrelsen Västerbotten who provided all the data and samples used through the EU financed project Kvarken Flada. A special thanks to Anniina Saarinen from there for always answering e-mails and helping me quickly and on short notice. Another special thanks to my supervisor Pär Byström for constructive feedback and helpful tips during the entire process. Without their help this project would not have been possible. Thanks to Sara for listening to me talk about fish an entire
semester.
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