Behavioural plasticity in a native species may be related to foraging resilience in the presence of an aggressive invader

Abstract

Competition between invasive and native species can result in the exploitation of resources by the invader, reducing foraging rates of natives. However, it is increasingly recognized that multiple factors can enhance the resilience of native species competing for limiting resources with invaders. Although extensively studied in terrestrial species, little research has focused on behavioural plasticity in aquatic ecosystems and how this influences native species resilience. Here, we examined the role of behavioural plasticity in interactions between a native Australian fish, Pseudomugil signifer, and a widespread invasive fish, Gambusia holbrooki. To determine whether P. signifer displays behavioural plasticity that may mitigate competition with G. holbrooki, we first quantified social behaviours (aggression, submission and affiliation) and shoal cohesion for each species in single- and mixed-species groups. Second, we compared the feeding rates of both species in these groups to ascertain if any modulation of social behaviours and cohesion related to foraging success. We found that aggressive and submissive behaviours of G. holbrooki and P. signifer showed plasticity in the presence of heterospecifics, but social affiliation, shoaling and, most importantly, foraging, remained inflexible. This variation in the degree of plasticity highlights the complexity of the behavioural response of a native species and suggests that both behavioural modulation and consistency may be related to sustaining foraging efficiency in the presence of an invader.

1. Introduction

Biological invasions are a major driver of global biodiversity loss, with adverse impacts on native populations [1]. When foraging niches overlap, competition can result in the exploitation of resources by the invader [2–4] and reduced foraging rates of natives [5]. However, it is becoming clear that multiple factors can serve to enhance the resilience of native species when competing for limiting resources, such as elevated intraspecific competition in invasive species [3], altered habitat use by natives [6] or abiotic factors, such as salinity or temperature, which can modulate competitive interactions between native and invasive species [7,8].

One well-documented factor that may enhance the resilience of native species is their capacity to modulate behaviours in response to the presence of invasive species. If native species are able to shift their behaviours appropriately, individual fitness may improve, promoting the persistence of the population. Appropriate adjustment of behaviours may include using an alternative food source [9] or increasing submissive/aggressive or avoidance behaviours [10,11]. Indeed, in some cases, behavioural plasticity has proven essential for the coexistence of invasive and native species and the survival of native populations (e.g. [12,13]).

Although extensively studied in terrestrial species, there has been little research on the role of behavioural plasticity in species resilience in aquatic ecosystems. Here, we examined the role of behavioural plasticity using the native Australian Pacific blue-eye, Pseudomugil signifer, and the globally invasive Eastern mosquito fish, Gambusia holbrooki. These fish species occupy the same streams along the east coast of Australia [14,15] and are surface feeders that target similar prey items at comparable [16,17] or reduced rates for P. signifer [15,18]. Additionally, both form social groups with conspecifics [19]. Numerous studies have suggested that the presence of G. holbrooki is detrimental to P. signifer, either in the form of reduced growth and fecundity [20] or via direct aggression, predation and competition [15,21,22]. It is also known that G. holbrooki displays behavioural plasticity (e.g. [23]), yet it is not well known whether P. signifer has the capacity for behavioural plasticity nor if such plasticity could mitigate the adverse effects of G. holbrooki (i.e. aggression and competition).

To examine whether P. signifer displays behavioural plasticity in the presence of G. holbrooki, we first quantified three key social behaviours (aggression, submission and affiliation) and shoal cohesion for each species in single- and mixed-species groups of six individuals. Second, we examined the feeding rate of both species in these groups to ascertain if modulation of social behaviours and cohesion aligned with foraging success. We compared social and foraging behaviours in single- versus mixed-species groups of the same density to disentangle the relative strengths of intra- versus interspecific competition and thereby elucidate the effect of G. holbrooki on P. signifer [24–26].

2. Methods

This study was conducted between September 2018 and January 2019 at the University of Wollongong, NSW, Australia. Gambusia holbrooki (n = 93) were collected from ponds on campus using hand nets. Only females were collected (sexed via inspection of anal fin; [19]) to avoid mating behaviours associated with males. Adult female P. signifer (N = 169) were obtained from a live fish supplier (www.livefish.com.au) (sexed via inspection of dorsal fins on arrival; [27]). As individuals used for this study originate from different rearing histories, some behavioural differences may arise as a result. All fish were maintained in housing aquaria (60 × 30 × 30 cm) for approximately two weeks to allow for acclimation to laboratory conditions prior to the start of trials.

To quantify social behaviours, three treatments were established each consisting of replicated groups: (i) G. holbrooki only (N = 6 fish per group; N = 10 groups), (ii) P. signifer only (N = 6 fish per group; N = 10 groups) and (iii) G. holbrooki and P. signifer mixed groups (N = 3 fish per species per group; N = 10 groups). In treatments 1 and 2, three fish were randomly selected as ‘focal fish' to be observed for behavioural scoring. In treatment 3, the behaviours of all fish, i.e. three G. holbrooki and three P. signifer, were scored. Fish were size-matched to within 10 mm of each other (G. holbrooki: 25.6 ± 0.651 mm; P. signifer: 26.1 ± 0.446 mm) and simultaneously placed into a test aquarium (60 × 30 × 30 cm) to form the treatment group to which they were assigned. Fish were allowed to acclimate to the test environment and observer presence for 5 min. Observations of focal fish were made in the morning and afternoon by one observer (M.L.K.) positioned directly in front of the test aquarium. The observation of treatments was conducted in the same order for both morning and afternoon observations, but in a different, randomized order the next observation day. Each focal fish was observed for 10 min and behaviours scored using a previously developed ethogram (electronic supplementary material, table S1a,b). An average count per behaviour was calculated from the morning and afternoon observation periods for each focal individual.

To quantify shoal cohesion, the test aquarium was subdivided into four equal-sized zones by marking the external surface of the front glass panel (electronic supplementary material, figure S1). A video camera (GoPro Hero 3+) was mounted directly in front of the aquarium using a tripod and each group was recorded for 30 min. Shoal cohesion was then calculated from the video by counting the number of focal fish in each zone at 3 min intervals. An average shoal standard deviation was then calculated from the zone counts, to produce one standard deviation per species per shoal (mixed-species groups had two cohesion values, i.e. one for each species; electronic supplementary material, figure S1a). Cohesion data were then categorized as low (less than 1) and high (greater than 1) for statistical analysis (electronic supplementary material, figure S1b), with a high standard deviation indicating high cohesion and vice versa for low standard deviation.

Immediately following observation of social behaviours and cohesion, the same groups underwent foraging trials to quantify foraging success. Six food pellets (New Life Spectrum Thera formula) were dropped into the water at the centre of the tank and the number of pellets consumed by each focal fish was determined by visual observations (M.L.K.) and later verified by video recordings taken simultaneously. After the completion of foraging trials, all fish were placed back into the housing tanks (separate housing tanks for used and unused fish) and the entire procedure replicated using new fish for each successive trial.

All statistics were performed using RStudio 3.5.1 [28]. A general linear mixed effects model was used to analyse the effects of group type (single or mixed species), species (G. holbrooki or P. signifer) and their interaction on average aggression, submission, social affiliation, shoal cohesion and foraging score (all log transformed except for social affiliation). Group ID was entered as a random effect. A generalized linear model with species, shoal type and their interaction on shoal cohesion (binary) was used to analyse shoal cohesion in mixed- and single-species groups. Normality of residuals was assessed via visual inspection of QQ plots.

3. Results

In both single- and mixed-species groups, G. holbrooki was significantly more aggressive than P. signifer, and both species displayed more aggression in mixed- than single-species groups (table 1 and figure 1a). Consequently, P. signifer displayed more submission in mixed- than single-species groups (in fact it rarely displayed submission among conspecifics alone), while G. holbrooki displayed more submission overall regardless of group type (table 1 and figure 1b). Overall, P. signifer performed more socially affiliative behaviours than G. holbrooki, both in the presence and absence of the invader (table 1 and figure 1c). For P. signifer, shoal cohesion remained constant regardless of treatment, but for G. holbrooki, cohesion was significantly higher in single- than mixed-species groups (table 1 and figure 1d). Finally, G. holbrooki and P. signifer foraged at similar rates, and there was no effect of group type on foraging rate for either species (table 1 and figure 1e).

Table 1.

General and generalized (*) linear mixed model outputs examining the effects of species and group type on social behaviours, foraging and cohesion from G. holbrooki and P. signifer. Group ID was a random effect in all models.

	model	d.f.	d.f. denom.	F value	p value
aggression	species	1	68.8	7.18	0.00923
	group type	1	28.4	27.2	<0.0001
	interaction	1	68.8	2.69	0.105
submission	species	1	51	27.2	0.00116
	group type	1	23.6	18.2	0.000280
	interaction	1	51	20.9	<0.0001
social affiliation	species	1	95.8	31.7	<0.0001
	group type	1	25.3	3.65	0.0675
	interaction	1	95.8	1.57	0.213
shoal cohesion*	species	1	38	48.39	0.489
	group type	1	37	43.90	0.0340
	interaction	1	36	39.54	0.0368
foraging	species	1	116	0.239	0.626
	group type	1	116	0.527	0.470
	interaction	1	116	1.612	0.207

Figure 1.

The relationship between behavioural interactions, species and group types. Mean count of (a) aggressive behaviours of G. holbrooki and P. signifer in single- and mixed-species groups, (b) submissive behaviours of G. holbrooki and P. signifer in single- and mixed-species groups, and (c) social affiliation of G. holbrooki and P. signifer in single- and mixed-species groups. (d) Mean shoal cohesion of G. holbrooki and P. signifer in single- and mixed-species groups, and (e) mean foraging rate of G. holbrooki and P. signifer in single- and mixed-species groups. Dashed lines represent P. signifer, solid lines represent G. holbrooki. Error bars are ± standard error (N = 120). (*) indicates a significant main effect; (**) indicates a significant interaction term.

4. Discussion

Here, we investigated whether P. signifer modulates its behaviours in the presence of G. holbrooki, and if this plasticity is likely to improve the resilience of this native species in the presence of the invader. We found that some behaviours, namely displays of aggression and submission by both species, differed in the presence of con- versus heterospecifics. However, other behaviours, namely social affiliation, shoal cohesion and foraging efficiency, remained consistent. Although the precise mechanism is not understood, it is possible that foraging efficiency of the native may be related to a combination of behavioural modulation and behavioural inflexibility.

Increased aggression to hetero- compared with conspecifics can benefit invaders by facilitating resource domination and range expansion [29,30]. In our study both the native and invader became more aggressive in mixed-species groups compared with single-species groups, although, overall, aggression by G. holbrooki was greater than that from P. signifer. However, this is not always the case for G. holbrooki (see [26]), and such variation in levels of intra- versus interspecific aggression between native and invasive species can be a function of overall group density [26] as well as relative body size [31]. Further research into the context dependency of aggression from G. holbrooki to con- and heterospecifics is needed. Furthermore, P. signifer displayed significantly more submissive acts in mixed-species groups (compared with rarely ever in single-species groups). This elevation in submissive behaviour by P. signifer therefore suggests that aggressive and submissive behaviours are both relatively plastic when it comes to interactions between these native and invasive species.

Despite fluctuations in aggressive and submissive behaviours between mixed- and single-species groups, socially affiliative behaviours by both species did not vary with respect to group type. The only source of significant variation was between the two species, with P. signifer exhibiting more social affiliation than G. holbrooki in general. Additionally, the cohesiveness of P. signifer shoals did not differ between group types, whereas the cohesiveness of G. holbrooki shoals was reduced in mixed-species groups. These findings indicate that unlike G. holbrooki, P. signifer remain highly affiliative with conspecifics regardless of group type, and that the level of shoal cohesion exhibited by P. signifer is unaffected by the presence of heterospecifics. However, as responses to heterospecifics frequently differ with species identity, it would be highly valuable to assess P. signifer behaviour in response to native heterospecifics to provide a comparison with responses to G. holbrooki in this study.

Foraging rates by G. holbrooki and P. signifer did not differ from each other nor in relation to group type. This was surprising given that G. holbrooki tends to dominate native species in regards to competition for food [32] and shows significantly more aggression than P. signifer in general. One hypothesis for sustained foraging rates by P. signifer is that despite the presence of aggressive G. holbrooki, behavioural shifts in aggression and submission in combination with behavioural consistency and inflexibility in social affiliation and shoal cohesion enabled P. signifier to continue to forage effectively. Indeed highly cohesive shoals display more efficient information transfer [33,34] which may in turn influence foraging success [35]. However, this result is based on a lack of difference in foraging, and hence should be treated with caution, and further work tracking the same individuals over multiple contexts (mixed- and single-species groups) and relating experimental changes in social behaviour to foraging would be important for validating this hypothesis.

While there may be benefits from sustained sociality and cohesion in the short term, long-term effects of G. holbrooki may be negative for the native owing to costs associated with elevating aggressive and submissive behaviours. Therefore, future research aimed at examining long-term effects on growth, fecundity and survivorship, in groups of different composition and densities, are needed to fully understand the interactions between invasive and native species and the ecological outcomes of these interactions.

Ethics

This study was conducted in accordance with an approved animal ethics protocol no. 18/11 from the University of Wollongong.

Data accessibility

The datasets supporting this article have been uploaded to Dryad and are available at: https://doi.org/10.5061/dryad.547d7wm70 [36].

Authors' contributions

M.L.K. carried out the collection of fish, fish husbandry, collection and analysis of data, and assisted with experimental design and drafting of the manuscript; M.Y.L.W. assisted with conceptual development, experimental design, fish husbandry and drafting of the manuscript; K.C.P. assisted with conceptual development, experimental design, fish husbandry and drafting of the manuscript; L.K.L. assisted with conceptual development, experimental design and drafting of the manuscript. All authors approved the final version of the manuscript and they agree to be held accountable for the work performed therein.

Competing interests

We declare we have no competing interests.

Funding

This project was funded by the Centre of Sustainable Ecosystems Solutions in the School of Earth, Atmospheric and Life Sciences at the University of Wollongong.