Omega-3 fatty acids accelerate fledging in an avian marine predator: a potential role of cognition

Abstract

Consuming omega-3 fatty acids (n-3 LCPUFAs) during development improves cognition in mammals, but the effect remains untested in other taxa. In aquatic ecosystems, n-3 LCPUFAs are produced by phytoplankton and bioaccumulate in the food web. Alarmingly, the warming and acidification of aquatic systems caused by climate change impair n-3 LCPUFA production, with an anticipated decrease of 80% by the year 2100. We tested whether n-3 LCPUFA consumption affects the physiology, morphology, behaviour and cognition of the chicks of a top marine predator, the ring-billed gull. Using a colony with little access to n-3 LCPUFAs, we supplemented siblings from 22 fenced nests with contrasting treatments from hatching until fledging; one sibling received n-3 LCPUFA-rich fish oil and the other, a control sucrose solution without n-3 LCPUFAs. Halfway through the nestling period, half the chicks receiving fish oil were switched to the sucrose solution to test whether n-3 LCPUFA intake remains crucial past the main growth phase (chronic versus transient treatments). Upon fledging, n-3 LCPUFAs were elevated in the blood and brains of chicks receiving the chronic treatment, but were comparable to control levels among those receiving the transient treatment. Across the entire sample, chicks with elevated n-3 LCPUFAs in their tissues fledged earlier despite their morphology and activity levels being unrelated to fledging age. Fledging required chicks to escape fences encircling their nest. We therefore interpret fledging age as a possible indicator of cognition, with chicks with improved cognition fledging earlier. These results provide insight into whether declining dietary n-3 LCPUFAs will compromise top predators' problem-solving skills, and thus their ability to survive in a rapidly changing world.

Keywords: Aquatic ecosystem; Bird; Brain development; Docosahexaenoic acid; Eicosapentaenoic acid; Essential fatty acid.

Fig. 1.

Photographs of the fenced nests, gavage procedure and string-pull test apparatus. (A) Fences deployed around nests were initially at a height of 15 cm above the ground and were raised gradually to 90 cm thereafter. An open string-pull task box allowed chicks to habituate to the test apparatus, and two clay planter pots provided hiding places. (B) Gavage of chicks using a syringe. The same technique was used for fish oil and sucrose solution supplementations. (C) The enclosure used for the string-pull test in relation to the nest of the chick being tested. The front of the enclosure was semi-transparent to permit interaction with the parents at the nest. While one sibling was undergoing a trial, other siblings were kept under a meshed container (yellow) that allowed communication with the parents but prevented the siblings from viewing the trial. Two cameras recorded each trial and foam mats (not pictured) were laid on top of the cameras during a trial to prevent gulls from flying into the enclosure. (D) Chick in front of the string-pull box while undergoing the string-pull test. Two sausage pieces were laid on either side of the string and a third piece was left in the box, accessible only by pulling on the string.

Fig. 2.

Incorporation of omega-3 fatty acids (n-3 LCPUFAs) into red blood cells (RBCs). The concentration of two n-3 LCPUFAs (docosahexanoic acid, DHA; eicosapentaenoic acid, EPA) was measured in the RBCs of 36 chicks at 15 (open circles) and 36 days post-hatching (dph; filled circles). Values are expressed as relative concentration (percentage of total identified fatty acids) and compared among three dietary treatments: chronic oil, transient oil and sucrose solution control. Each mean (small circle) is presented with its 95% confidence interval and raw data (large circles). Age groups within a treatment are significantly different when the letters above their confidence intervals are of different case, and treatment groups are significantly different when they do not share the same letters (Tukey post hoc tests).

Fig. 3.

Incorporation of n-3 LCPUFAs into RBCs predicts incorporation of n-3 LCPUFAs into the cerebral hemispheres of the brain. The concentrations of two n-3 LCPUFAs (DHA and EPA) were measured from the RBCs of 12 chicks at 36 dph and from the cerebral hemispheres of the same chicks at 42 dph, and are expressed as relative concentration (percentage of total identified fatty acids). The relationships (±s.e.) between the concentrations of n-3 LCPUFAs in both tissues, as predicted by our models, are represented by a black line (with grey shading). Raw data are represented by the points, with colours and shapes corresponding to the treatment groups (orange circles, sucrose solution control; green triangles, transient oil; blue squares, chronic oil; n=4 for each).

Fig. 4.

Chicks with more DHA fledged earlier. Fledging age was measured as the number of days before 42 dph, which was assigned as the maximum age of fledging in our study. Concentrations of two n-3 LCPUFAs (DHA and EPA) were measured in RBCs at 36 dph and expressed as relative concentration (percentage of total identified fatty acids). This model is based on a sample size of 33 chicks, as two were attacked and died in their nest before fledging (38 dph for both) and one from the chronic oil treatment fledged early at 34 dph and by 37dph but could not be captured for a blood sample at 36 dph. The predicted relationships (±s.e.) are represented by a black line (with grey shading). Treatment, which was analysed separately from the concentrations of DHA and EPA in the RBCs (right panel), did not have a significant effect on fledging age (n=34 chicks). Each mean (small circle) is presented with its 95% confidence interval. Raw data are represented by the points, with colours and shapes corresponding to the treatment groups (orange circles, sucrose solution control N=13; green triangles, transient oil N=11; blue squares, chronic oil N=9 for the DHA+EPA model, N=10 for the treatment model).

Fig. 5.

Mass gained during the nestling period in the three dietary treatment groups. Growth was measured by weighing the chicks (N=10 chronic oil, N=11 transient oil, N=15 sucrose solution control) daily from hatching until 23 dph and weekly afterwards until fledging. The mean growth trajectories are represented by the lines (±s.e. shading), modelled using the average non-parametric local weighted regression of each dietary treatment group. Raw data are represented by the points, with colours and shapes corresponding to the treatment groups (orange circles, sucrose solution control; green triangles, transient oil; blue squares, chronic oil). The linear growth phase occurred between 5 and 22 dph and the growth curves appear identical to growth curves of unsupplemented ring-billed gulls published in previous studies (Chardine, 1978; Dawson et al., 1976; Iacovides and Evans, 1998; Oswald et al., 2013).

Fig. 6.

DHA in RBCs is negatively related to ALA and positively related to EPA. The concentrations of DHA, α-linolenic acid (ALA) and EPA were measured in RBCs at 36 dph (n=35 chicks, as one chick from the chronic group fledged before a blood sample could be taken at 36 dph) and expressed as relative concentration (percentage of total identified fatty acids). The predicted relationships (±s.e.) are represented by a black line (with grey shading). Raw data are represented by the points, with colours and shapes corresponding to the treatment groups (orange circles, sucrose solution control N=15; green triangles, transient oil N=11; blue squares, chronic oil N=9).