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Planktivore vertical migration and shoaling under a subarctic light regime

TL;DR: Visually foraging planktivorous fish are prey of visual predators as mentioned in this paper, and their foraging behavior may be affected by light levels both in terms of gain and risk.
Abstract: Visually foraging planktivorous fish are prey of visual predators, and their foraging behaviour may be affected by light levels both in terms of gain and risk. The large seasonal change in day leng...

Summary (4 min read)

Introduction

  • Light is important for visually oriented predators as darkness provides cover for their prey, and behavioural responses to changes in light intensity are often associated with predator-prey interactions (Blaxter 1975; Helfman 1993; Pitcher and Parrish 1993) .
  • A predator increasing its foraging activity will simultaneously increase its predation risk, and there is therefore a tradeoff between foraging gain and predation risk (Gilliam and Fraser 1987; Lima and Dill 1990) .
  • In some planktivorous fish species, swimming activity has been observed to be highest in crepuscular light (Batty 1987; Iida and Mukai 1995; Gjelland et al. 2004) .
  • By contrasting day and night samples from June, August, and September, the authors investigated how behavioural traits relate to the changing light regime, i.e. both within the diel cycle and during the ice-free season.

Methods

  • In order to evaluate DVM and shoaling patterns in planktivorous coregonids, the authors combined echosounding techniques with gillnetting for planktivores, planktivore diet analysis, and zooplankton sampling in a high latitude lake at periods of contrasting differences in the diel light cycle.
  • Published literature on coregonid reactive distance and salmonid piscivore reactive distance in relation to light intensity were used to evaluate the influence of light level on the foraging opportunity and predation risk for the studied planktivores.

Study site and fish community

  • The pelagic fish community of the oligotrophic Lake Skrukkebukta was sampled around the 20 th of June, August, and September 2000.
  • The ice-free season in the watercourse lasts from the end of May or beginning of June to October -November.
  • Two morphs of whitefish have been described: a pelagic densely-rakered (DR) morph, which forages predominantly on zooplankton, and a larger benthic-dwelling sparsely-rakered (SR) morph, which forages on benthic prey (Amundsen et al. 2004; Østbye et al. 2006) .
  • DR whitefish and vendace are the dominant pelagic fish in the Pasvik watercourse (Bøhn and Amundsen 2001; Gjelland et al. 2007) , with brown trout being the dominant pelagic predator (Bøhn et al.
  • About 1000 of these fish are released into Skrukkebukta.

Reactive distance relative to light

  • In order to develop a reactive distance model of visual foraging in coregonid planktivores, the authors analyzed data on Coregonus artedi reactive distance in relation to prey size (Link 1998 ) and light intensity (Link and Edsall 1996) .
  • The authors found that there was a constant relationship.
  • The full coregonid reactive distance model as a function of light and prey size can now be given (Fig. 2d , Eq. 6, prey length and reactive distance in m).
  • The species-specific reactive distance may differ at a given light intensity, but the shape of the reactive distance to light relationship is remarkably similar and there is no further increase in the reactive distance above approximately 18 lux for any of the species.
  • The shape of the reactive distance model was little influenced by the turbidity.

Light measurements

  • The light extinction coefficient k was estimated from light profiles sampled in 0.5 m intervals during June and August.
  • Surface illumination (unit lux) was estimated using hourly averaged global irradiation data (Wm -2 ) from Bioforsk Soil and Environment Division, Svanhovd research station, situated about 10 km from the study lake.
  • The exact conversion between Wm -2 and lux depends inter alia on weather and sun elevation.
  • For the August and September nights, when light level was too low for global irradiation measurements, the Janiczek and DeYoung (1987) model was used to estimate the surface illumination in lux.

Zooplankton sampling

  • Zooplankton samples were collected using a 30 l Schindler-Patalas trap with 65µm mesh size.
  • In the laboratory, all crustacean individuals in the daytime samples were counted and identified to species or genus, other prey taxa were identified to family level.
  • Only cladocerans were counted in the night-time samples.

Biological sampling

  • The relationship between target strength TS (the logarithmic domain of acoustic backscattering area, positively related to fish size) and fish length normally use total length LT of the fish (Simmonds and MacLennan 2005) .
  • LT was found by multiplying LF with 1.08, a conversion factor found from subsamples of both coregonid species in the catches.
  • The age of the coregonids was read from whole otoliths (Skurdal et al. 1985) .
  • Prey items in the coregonid stomachs were categorized as Bosmina, Daphnia, Cyclopoida, Calanoida, benthic invertebrates, insect pupae, or surface insects.
  • The stomach fullness was subjectively determined on a scale from 0 to 100 % (full), and the contribution of each prey category to the total volume of the stomach content was likewise determined.

Acoustic sampling

  • To monitor and evaluate swimming behaviour of pelagic fish, sampling was performed using acoustics with a combination of mobile vertical (down-looking beam, oriented 90° from surface) and horizontal (side-looking beam, oriented approximately 5° from surface) techniques around midnight and mid-day (Fig. 1b ).
  • The down-looking acoustics were used to quantify fish depth distributions, depth of shoals, and fish density estimation.
  • Only transects parts covering depths greater than 15 m were used, with a degree of coverage c = 3 (Aglen 1983) for each of the side-and downlooking surveys.
  • The length of the acoustic pulse (0.44 m) was subtracted from the lower range.

Reactive distance

  • The reactive distance relationship to light produced by the planktivore coregonid reactive distance model (Eq. 6) differed somewhat in shape from that of the piscivore salmonids reactive distance model (Eq. 7) (Fig. 2d ).
  • But the two models also share a similarity in that.

Gillnet catches and fish density

  • A total of 330 fish were caught in the pelagic gillnets.
  • Of these, 10 SR whitefish and 1 pike was excluded from the further analyses.
  • DR whitefish dominated the catches in all months.
  • The pelagic coregonid fish community consisted of small individuals with modal lengths of approximately 10 cm for both vendace and DR whitefish (Table 2 ).
  • The pelagic fish density in September was estimated to 1799 fish ha -1 (range 801 to 3197 for the 95 % lower and upper confidence intervals, respectively) by the Sv/TS scaling method.

Zooplankton distribution and coregonid diet

  • The highest daytime zooplankton densities were found close to the surface in all sampling months.
  • Around midnight, the vertical distributions of Bosmina and Daphnia were relatively even, whereas the depth distribution of both these species was skewed towards the surface during mid-day (Fig. 3 ).
  • This indicated that there was a tendency towards reversed DVM in these two zooplankton species.
  • The order of importance of the prey categories found in coregonid stomachs was Bosmina, chironomid pupae, Daphnia, surface insects, Cyclops scutifer, Leptodorea kindti, and with benthic prey items such as Chydorus and chironomid larvae as the least important of included prey items (Fig. 3 ).
  • The coregonid stomach fullness was least in June, and increased towards September (Fig. 3 ).

Diel vertical migration and shoaling patterns

  • There was a consistent pattern of vertical migration, with day vertical fish distributions being deeper than midnight distributions in all months (Fig. 4 ).
  • The difference in the centre of gravity Dcg between day and midnight depth distributions in June was only 1.2 m and not significant (Tukey test, P=0.77), as seen with the down-looking surveys (Fig. 4 ).
  • The increased depth of the day vertical fish distributions towards August and September was stronger than the increased light penetration (Fig. 4 ).
  • The distribution peaks were below the 0.4 lux light level in August and September (Fig. 4 .
  • This pattern was seen both with the down-looking and side-looking surveys.

Discussion

  • The authors findings show that DVM behaviour in coregonids consistently varied with changes in the day-night light cycle.
  • Deeper day-time than night-time distributions of the fish were observed in all months, and the range of the DVM increased with increasing differences in light levels between night and day from June to September.
  • The pattern of a more extensive DVM as differences between day and night light levels increased supports the hypothesis that DVM is strongly influenced by the light level (Blaxter 1975) .
  • The optimal trade-off between foraging and predation risk is thus argued to be state dependent (Lima and Dill 1990; Milinski 1993; Lima 1998b) , although field evidence is sparse.
  • The planktivore coregonids avoided light levels below the light threshold for visual foraging inferred from foraging experiments in other coregonids, suggesting a preference for a visual foraging mode.

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1
Planktivore vertical migration and shoaling under a subarctic 1
light regime 2
3
Karl Øystein Gjelland, Thomas Bøhn, John K. Horne, Ingrid Jensvoll, Frank Reier Knudsen, 4
and Per-Arne Amundsen 5
6
K. Ø. Gjelland
1
. Norwegian College of Fishery Science, University of Tromsø, N-9037 7
Tromsø, Norway. 8
Thomas Bøhn
2
. Norwegian College of Fishery Science, University of Tromsø, N-9037 9
Tromsø, Norway. 10
John K. Horne. School of Fishery and Aquatic Sciences, University of Washington, Box 11
355020, Seattle, WA 98195-5020, USA. 12
Ingrid Jensvoll. Norwegian College of Fishery Science, University of Tromsø, N-9037 13
Tromsø, Norway. 14
Frank Reier Knudsen. Simrad, Box 111, 3191 Horten, Norway. 15
Per-Arne Amundsen. Norwegian College of Fishery Science, University of Tromsø, N-9037 16
Tromsø, Norway. 17
18
19
1
Corresponding author (Email: Karl.Gjelland@nfh.uit.no) 20
2
Present address: GenØk Centre for Biosafety, N-9037 Tromsø, Norway 21
22
23

2
Abstract: Visually foraging planktivorous fish are prey of visual predators, and their foraging 24
behaviour may be affected by light levels both in terms of gain and risk. The large seasonal 25
change in day length throughout a subarctic summer at 69° N was used to show the influence 26
of light on diel vertical migration (DVM) and shoaling patterns in a planktivorous fish 27
assemblage consisting two species (Coregonus lavaretus and C. albula). Under the midnight 28
sun in June, night and day-time behaviour was similar with extensive shoaling and limited 29
DVM. With increasingly darker nights towards autumn, the fish dispersed during the dark 30
hours and showed more extensive DVM. Throughout the changing light regime of both the 31
day and the season, the planktivores consistently chose depths with light levels compatible 32
with visual foraging and reduced predation risk as revealed from reactive distance modelling 33
of coregonids and their salmonid predators. The findings support the hypothesis that 34
behavioural decisions are based on a trade-off between foraging rate and predation risk, and 35
increased predator avoidance behaviour towards autumn suggested that this trade-off is state-36
dependent. 37
38
Keywords: Planktivory; piscivory; predator-prey; trade-off; state-dependence 39
40

3
Introduction 41
Light is important for visually oriented predators as darkness provides cover for their prey, 42
and behavioural responses to changes in light intensity are often associated with predator-prey 43
interactions (Blaxter 1975; Helfman 1993; Pitcher and Parrish 1993). The non-consumptive 44
effects (non-lethal, e.g. reduced growth and birth rates) of a predator on its prey population 45
may be as important as the consumptive effects (i.e. removal of individuals) in population 46
regulation, and are often transmitted through dynamic traits such as behaviour of individuals 47
in the prey population (Lima 1998a; Preisser et al. 2005; Pangle et al. 2007). The effect of 48
modified traits may cascade to the resource populations of the prey (trait mediated indirect 49
interactions, i.e. effects of a predator on a receiving species is mediated through a transmitter 50
species, Dill et al. 2003; Werner and Peacor 2003). Knowledge of behavioural patterns is 51
therefore crucial to understand community dynamics. In many fish species, behavioural traits 52
such as diel vertical migration (DVM), shoaling, and swimming activity have been associated 53
with predator-prey interactions and shown to be correlated to light intensity changes (Blaxter 54
1975; Helfman 1993; Pitcher and Parrish 1993). 55
Light intensity influences the visual acuity of prey and predator, affecting both predator 56
efficiency and predator recognition in prey. The encounter rate and resulting feeding rate of a 57
visual predator is a function of light intensity, prey availability, prey visibility, and activity 58
levels of both predator and prey (Eggers 1977; Evans 1989). A predator increasing its 59
foraging activity will simultaneously increase its predation risk, and there is therefore a trade-60
off between foraging gain and predation risk (Gilliam and Fraser 1987; Lima and Dill 1990). 61
This trade-off may be state-dependent as animals that are either food-deprived or has a low 62
reproductive value are expected to take higher risks than satiated animals or animals close to 63
reproduction (Milinski 1993; Clark 1994; Damsgård and Dill 1998). 64

4
DVM-patterns observed for some planktivorous fish species support the trade-off 65
hypothesis between foraging gain and predation risk (Clark and Levy 1988; Scheuerell and 66
Schindler 2003; Hrabik et al. 2006). In aquatic environments, light intensity decreases with 67
increasing depth and turbidity. During light hours, fish may reduce activity or migrate to 68
deeper, darker and safer habitats to reduce predation risk. During darkness hours when 69
predation risk from visually oriented predators is reduced, they may safely return to the 70
surface waters where food is normally most abundant. Other hypotheses explaining DVM 71
suggest that planktivorous fish track the DVM of their prey (Janssen and Brandt 1980; 72
Eshenroder and Burnham-Curtis 1999), or that it is caused by bioenergetic benefits when 73
there is a separation between the habitat optimal for foraging and the habitat optimal for 74
growth (Brett 1971; Wurtsbaugh and Neverman 1988; Sims et al. 2006). 75
Predation risk have also influenced the evolution of shoaling (Pitcher and Parrish 1993). 76
Improved predator detection, recognition, and avoidance is an important motivator to form 77
shoals, although foraging gain may be reduced due to intra-shoal competition for food (Lima 78
and Dill 1990; Magurran 1990; Pitcher and Parrish 1993). Shoaling reduces the probability of 79
being preyed on, and the rapid, coordinated movement by shoals serves to protect individual 80
members (Magurran 1990; Pitcher and Parrish 1993). Shoaling is recognized as an important 81
anti-predator behaviour, and represents an alternative or supplementary defence strategy to 82
DVM for pelagic fish. 83
Changes in activity patterns and vertical use of habitat typically occur during crepuscular 84
periods (Blaxter 1975; Helfman 1993; Pitcher and Parrish 1993). In some planktivorous fish 85
species, swimming activity has been observed to be highest in crepuscular light (Batty 1987; 86
Iida and Mukai 1995; Gjelland et al. 2004). Periodic changes in behaviour may also be 87
influenced by endogenous circadian rhythms as well as changes in light (Thorpe 1978), but 88
these factors are often confounded since circadian rhythms typically have the same periodicity 89

5
as the day-night cycle. At latitudes above the polar circle, however, the sun is above the 90
horizon for 24 hrs a day during midsummer. Later in the season dark nights approach, and by 91
autumnal equinox in September nights are as long as days. High latitude locations therefore 92
provide excellent natural conditions for testing the light dependence of behavioural traits. 93
The objective of this study was to evaluate the effect of diel and seasonal changes in light 94
intensity on DVM and shoaling patterns of planktivorous whitefish Coregonus lavaretus (L.) 95
and vendace Coregonus albula (L.) combined in a subarctic lake in the Pasvik watercourse, 96
northern Norway. These co-existing planktivores are predated on by piscivorous brown trout 97
(Salmo trutta L.) (Kahilainen and Lehtonen 2002; Jensen et al. 2004, 2008). By contrasting 98
day and night samples from June, August, and September, we investigated how behavioural 99
traits relate to the changing light regime, i.e. both within the diel cycle and during the ice-free 100
season. Specific hypotheses regarding the coregonid behaviour included: (1) DVM will be 101
limited or absent in June under the midnight sun, but extensive after the onset of dark nights 102
in August and September; (2) shoaling will be observed over 24 hrs in June, but only during 103
daylight hours in August and September; (3) planktivorous fish choose depths with sufficient 104
light for visual foraging, but with reduced predation risk; (4) the predator avoidance 105
behaviour will be less pronounced in June after a long ice-covered winter, due to hunger and a 106
long time span to the late autumn reproduction as compared to later months. 107
Methods 108
In order to evaluate DVM and shoaling patterns in planktivorous coregonids, we combined 109
echosounding techniques with gillnetting for planktivores, planktivore diet analysis, and 110
zooplankton sampling in a high latitude lake at periods of contrasting differences in the diel 111
light cycle. Published literature on coregonid reactive distance and salmonid piscivore 112
reactive distance in relation to light intensity were used to evaluate the influence of light level 113
on the foraging opportunity and predation risk for the studied planktivores. 114

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  • ...For example, diel vertical migration is a behavioral strategy observed in many fish (Brett 1971; Gjelland et al. 2009; Hrabik et al. 2006), with diel shifts often linked to changes in diet and habitat use (Nunn et al. 2010)....

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TL;DR: This work has shown that predation is a major selective force in the evolution of several morphological and behavioral characteristics of animals and the importance of predation during evolutionary time has been underestimated.
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TL;DR: The nature of predation, the influence of population interactions on community structure, and Ecological applications at the level of communities and ecosystems are examined.
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  • ...…on its prey population 45 may be as important as the consumptive effects (i.e. removal of individuals) in population 46 regulation, and are often transmitted through dynamic traits such as behaviour of individuals 47 in the prey population (Lima 1998a; Preisser et al. 2005; Pangle et al. 2007)....

    [...]

  • ...The optimal 568 trade-off between foraging and predation risk is thus argued to be state dependent (Lima and 569 Dill 1990; Milinski 1993; Lima 1998b), although field evidence is sparse....

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  • ...This simple relationship has been extended to other 551 animals in the μ/f-rule (Lima 1998b), were f denotes foraging rate (Gilliam and Fraser 1987; 552 Clark and Levy 1988)....

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