Ontogenetic shift in plant-related cognitive specialization by a mosquito-eating predator

Abstract

Evarcha culicivora, an East African salticid spider, is a mosquito specialist and it is also a plant specialist, with juveniles visiting plants primarily for acquiring nectar meals and adults visiting plants primarily as mating sites. The hypothesis we consider here is that there are ontogenetic shifts in cognition-related responses by E. culicivora to plant odour. Our experiments pertain to cross-modality priming effects in three specific contexts: executing behaviour that we call the 'visual inspection of plants' (Experiment 1), adopting selective visual attention to specific visual targets (Experiment 2) and becoming prepared to respond rapidly to specific visual targets (Experiment 3). Our findings appear not to be a consequence of salient odours in general elevating E. culicivora's motivation to respond to salient visual stimuli. Instead, effects were specific to particular odours paired with particular visual targets, with the salient volatile plant compounds being caryophyllene and humulene. We found evidence that prey odour primes juveniles and adults to respond to seeing specifically prey, mate odour primes adults to respond to seeing specifically mates and plant odour primes juveniles to respond to seeing specifically flowers. However, plant odour appears to prime adults to respond to seeing specifically a mate associated with a plant.

Keywords: Cross-modality priming; Evarcha culicivora; Lantana camara; Salticidae; Selective attention; Spider.

Fig. 1

Apparatus for Experiments 1 and 2 (see text for details) when test spiders were adult males and females of Evarcha culicivora. Glass arena (internal dimensions: 100 mm × 100 mm, 37 mm high) was centred on top of a glass base (140 × 140 mm), which was in turn centred on top of a wooden arena table (300 mm × 300 mm; wood thickness, 17 mm) supported by four legs (each leg 40 mm × 40 mm in cross section and 250 mm in height). Metal braces held the four display chambers (inner dimensions 260 mm × 40 mm) tightly against the table top. Each display chamber had two wooden side walls (80 mm wide, wood thickness 20 mm). Each display chamber was centred on a wooden display-chamber table (length 300 mm × 80 mm; wood thickness, 20 mm), with a pair of wooden legs (height 220 mm) supporting each display-chamber table. For stability, each of these legs was bolted to the nearest leg of the arena table. A glass odour chamber (inner dimensions 70 mm × 70 mm × 70 mm) sat under the arena table. Air entered through a hole centred in the arena table top and through a corresponding inflow hole in the bottom of the arena, and air left the arena through an outflow hole centred in the arena lid (hole diameters 12 mm). There was a glass tube in the outflow hole and another glass tube in the inflow hole (inner diameter of each tube 11 mm, outer diameter 12 mm, length 20 mm).

Fig. 2

Apparatus for Experiments 1 and 2 (see text for details) when test spiders were juveniles of Evarcha culicivora. Glass arena (internal dimensions: 50 mm × 50 mm, 37 mm high) was centred on top of a glass base (56 mm × 56 mm), which was in turn centred on top of a wooden arena table (90 mm × 90 mm; wood thickness, 17 mm) supported by four legs (each leg 40 mm × 40 mm in cross section and 250 mm in height). Metal braces held the four display chambers (inner dimensions 100 mm × 100 mm) tightly against the table top. Each display chamber had two wooden side walls (80 mm wide, wood thickness 20 mm). Two grooves (3 mm wide, 40 mm apart) ran from the top to the bottom of each side wall and across the floor of the chamber. Each display chamber was centred on a wooden display-chamber table (length 90 mm × width 80 mm; wood thickness, 20 mm), with a pair of wooden legs (height 220 mm) supporting each display-chamber table. For stability, each of these legs was bolted to the nearest leg of the arena table. A hole (diameter 12 mm) was centred in the bottom of each display chamber and, correspondingly, in the display chamber table. A glass odour chamber (inner dimensions 70 mm × 70 mm × 70 mm) sat out of the test spider’s field of view. Air entered through a hole centred in the arena table top and through a corresponding inflow hole in the bottom of the arena, and air left the arena through an outflow hole centred in the arena lid (hole diameters 12 mm). There was a glass tube in the outflow hole and another glass tube in the inflow hole (inner diameter of each tube 11 mm, outer diameter 12 mm, length 20 mm).

Fig. 3

Apparatus for Experiment 3 (see text for details). Test spiders were always adult males of Evarcha culicivora. Glass arena (inside length 70 mm, inside height 37 mm) had three sectors, with the centre sector (30 mm × 25 mm) being narrower than the two side sectors (20 mm × 50 mm). The arena was centred on top of a glass base (80 mm × 80 mm), which was in turn centred on top of a wooden arena table (140 mm × 130 mm; wood thickness, 17 mm) supported by four legs (each leg 40 mm × 40 mm in cross section and 250 mm in height). Metal braces held both of the display chambers (inner dimensions 100 mm × 40 mm) tightly against the table top. Each chamber had two wooden side walls (80 mm wide, wood thickness 20 mm). Two grooves (3 mm wide, 40 mm apart) ran from the top to the bottom of each side wall and across the floor of the chamber. Each display chamber was centred on a wooden display-chamber table (length 140 mm × width 80 mm; wood thickness, 20 mm), with a pair of wooden legs (height 220 mm) supporting each display-chamber table. For stability, each of these legs was bolted to the nearest leg of the arena table. The height of the arena-table legs and display-table legs were such that the top of each chamber was 73 mm above the arena-table top. A hole (diameter 12 mm) was centred in the bottom of each display chamber and, correspondingly, in the display chamber table. A glass odour chamber (inner dimensions 70 mm × 70 mm × 70 mm) sat out of the test spider’s field of view. Air entered through a hole centred in the arena table top and through a corresponding inflow hole in the bottom of the arena, and air left the arena through an outflow hole centred in the arena lid (hole diameters 12 mm). There was a glass tube in the outflow hole and another glass tube in the inflow hole (inner diameter of each tube 11 mm, outer diameter 12 mm, length 20 mm).

Fig. 4

Mean response duration in trials for Experiment 1 using no odour (control) and caryophyllene odour. Error bars indicate SEM. Juveniles specified by body length (mm). For all test-spider categories, N = 20 test spiders. (A) Lantana camara used as the visual stimulus. (B) Three other plant species used as the visual stimulus. As no male-female differences were evident with other plants (A and C), only males were used as test spiders here. (C) Bougainvillea glaba used as the visual stimulus.

Fig. 5

Mean response duration in trials for Experiment 1 when only Lantana camara was used as the visual stimulus. Error bars indicate SEM. Note: data for caryophyllene odour and data for no odour (control) same as in Fig. 4(A). Juveniles specified by body length (mm). For all test-spider categories, N = 20 test spiders. (A) Other compounds (humulene and cineole) used as the odour source. (B) Prey used as the odour source. (C) Mates used as the odour source.

Fig. 6

Mean response duration in trials for Experiment 2 when using (A) cryptic Lantana camara flowers (all test-spider categories) and (B) conspicuous Lantana camara flowers (small juveniles only) as the visual stimulus. Odour sources vary. Error bars indicate SEM. Juveniles specified by body length (mm). For all test-spider categories, N = 20 test spiders. Note: control data for small juveniles presented with cryptic flowers in (B) the same as in (A).

Fig. 7

Mean response duration in trials for Experiment 2 when (A) using cryptic prey (all test-spider categories) and (B) conspicuous prey (males and small juveniles only) as the visual stimulus. Odour sources vary. Error bars indicate SEM. Juveniles specified by body length (mm). For all test-spider categories, N = 20 test spiders. Note: control data for males and small juveniles presented with cryptic prey in (B) the same as in (A).

Fig. 8

Mean response duration in trials for Experiment 2 when using (A) cryptic mates (males and females) and (B) conspicuous mates (males only) as the visual stimulus. Odour sources vary. Error bars indicate SEM. For all test-spider categories, N = 20 test spiders. Note: control data for males presented with cryptic mates in (B) the same as in (A).