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. 2023 Jan;7(1):82-91.
doi: 10.1038/s41559-022-01931-8. Epub 2023 Jan 5.

Terrestrial invasive species alter marine vertebrate behaviour

Rachel L Gunn  1 , Cassandra E Benkwitt  2 , Nicholas A J Graham  2 , Ian R Hartley  2 , Adam C Algar  3 , Sally A Keith  2
Affiliations

Terrestrial invasive species alter marine vertebrate behaviour

Rachel L Gunn et al. Nat Ecol Evol. 2023 Jan.

Abstract

Human-induced environmental changes, such as the introduction of invasive species, are driving declines in the movement of nutrients across ecosystems with negative consequences for ecosystem function. Declines in nutrient inputs could thus have knock-on effects at higher trophic levels and broader ecological scales, yet these interconnections remain relatively unknown. Here we show that a terrestrial invasive species (black rats, Rattus rattus) disrupts a nutrient pathway provided by seabirds, ultimately altering the territorial behaviour of coral reef fish. In a replicated ecosystem-scale natural experiment, we found that reef fish territories were larger and the time invested in aggression lower on reefs adjacent to rat-infested islands compared with rat-free islands. This response reflected changes in the economic defendability of lower-quality resources, with reef fish obtaining less nutritional gain per unit foraging effort adjacent to rat-infested islands with low seabird populations. These results provide a novel insight into how the disruption of nutrient flows by invasive species can affect variation in territorial behaviour. Rat eradication as a conservation strategy therefore has the potential to restore species interactions via territoriality, which can scale up to influence populations and communities at higher ecological levels.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Turf algal δ15N and turf algal cover around islands with seabirds and islands with invasive rats within the Chagos Archipelago.
a,c, Each point on the violin plots represents a single P. lacrymatus territory. Black bars show the mean estimates for turf algal δ15N (a, n = 27 around islands with seabirds, n = 29 around islands with rats) and for turf algal cover (c, n = 20 around islands with seabirds, n = 30 around islands with rats). Means ± s.d. are presented above each violin plot. The upper and lower bounds of the violin plots show the range of the raw data. b,d, Bayesian posterior densities show the effect of island invasion status on turf algal δ15N (b) and turf algal cover (d). Points are median estimates, with thick and thin lines representing 75% and 95% credible intervals, respectively. PPs, ERs and posterior densities in green show the extent to which nitrogen input (b) and turf algal cover (d) are higher around islands with seabirds. Rat and seabird graphics from PhyloPic.org under Public Domain Dedication 1.0 licences.
Fig. 2
Fig. 2. Variation in P. lacrymatus territory size between and within island invasion status type with turf algal δ15N and turf algal cover within the Chagos Archipelago.
a, Raw data showing territory size estimates for P. lacrymatus individuals (n = 30 around islands with seabirds, n = 30 around islands with rats). Each point represents a single P. lacrymatus territory. Black bars show the mean estimates for P. lacrymatus territory size, and mean ± s.d. are also presented above each violin plot. The upper and lower bounds of the violin plots show the range of the raw data. b, Bayesian posterior density showing the effect of island invasion status on P. lacrymatus territory size. Points are median estimates, with thick and thin lines representing 75% and 95% credible intervals, respectively. The PP, ER and posterior density in green show the extent to which P. lacrymatus territories are smaller around islands with seabirds. c,e, Relationships between turf algal cover (e), turf algal δ15N (c) and P. lacrymatus territory size within island invasion status type. Points are partialized residuals extracted from Bayesian models for each P. lacrymatus individual. Best fit lines are extracted from Bayesian model conditional effects, with grey shading indicating 75% quantiles around the mean estimate. d,f, Posterior density plots showing the strength of the relationships in c and e, respectively. Densities to the right of 0 indicate a positive relationship, while densities to the left of 0 indicate a negative relationship. Evidence ratios show how much more likely the observed relationship is present over the alternative (grey shading). Rat and seabird graphics from PhyloPic.org under Public Domain Dedication 1.0 licences.
Fig. 3
Fig. 3. P. lacrymatus aggression between and within island invasion status type with turf algal δ15N and cover within the Chagos Archipelago.
a, Raw aggression estimates for P. lacrymatus individuals (n = 28 around islands with seabirds, n = 29 around islands with rats). Each point represents a single P. lacrymatus territory. Black bars are mean estimates, and mean ± s.d. are also presented above each violin plot. The upper and lower bounds of the violin plots show the range of the raw data. b, Bayesian posterior density showing the effect of island invasion status on P. lacrymatus aggression. Points are median estimates, with lines representing 75% and 95% credible intervals, respectively. The PP, ER and posterior density in green show the extent to which P. lacrymatus aggression is higher around islands with seabirds. c,e, Relationships between turf algal cover (e), turf algal δ15N (c) and P. lacrymatus aggression within island invasion status type. Points are partialized residuals extracted from Bayesian models, with best fit lines extracted from Bayesian model conditional effects. Grey shading indicates 75% quantiles around the mean estimate. d,f, Posterior density plots showing the strength of the relationships in c and e, respectively. Densities to the right of 0 indicate a positive relationship, while densities to the left of 0 indicate a negative relationship. Evidence ratios show how much more likely the observed relationship is present over the alternative (grey shading). Rat and seabird graphics from PhyloPic.org under Public Domain Dedication 1.0 licences.
Fig. 4
Fig. 4. Threshold model of economic defendability with results for damselfish territoriality in the presence and absence of seabird nutrient subsidies.
Territoriality is predicted to occur where the benefits outweigh the cost (shaded blue area). Below the threshold of territoriality, there is predicted to be no relationship between resource value and territoriality (dashed red boxes). The presence of nutrient subsidies around islands with seabirds is predicted to increase resource value to damselfish, resulting in higher levels of aggression (green point) than around islands with invasive rats (orange point). An inverse relationship between resource value and territory size (secondary y axis) is also predicted such that territories of higher resource value, that is, those around islands with seabirds, will be smaller (circular bird icon) than territories with lower resource value, that is, around islands with invasive rats (circular rat icon). Around islands with rats, resource value is low, and variation in turf algal cover and turf algal δ15N is not enough to place P. lacrymatus individuals above the threshold of territoriality (orange arrows). Around islands with seabirds, elevated δ15N is high, placing P. lacrymatus territories beyond the threshold of territoriality (green arrow with open arrowhead). Variation in aggression within reefs adjacent to islands with seabirds is instead driven by variation in turf algal cover (green arrow with closed arrowhead). Rat and seabird graphics from PhyloPic.org under Public Domain Dedication 1.0 licences.
Extended Data Fig. 1
Extended Data Fig. 1. The location of study sites around the Chagos Archipelago.
The location of the Chagos Archipelago in the Indian ocean is shown in the inset. Surveys were conducted around three atolls: Peros Banhos (PB), Salomon (SAL) and the Great Chagos Bank (GCB). Points represent the locations of the 10 reefs where surveys were conducted.
Extended Data Fig. 2
Extended Data Fig. 2. The relationship between turf algal cover and δ15N within P. lacrymatus territories.
Top: Points represent partialized residuals extracted from Bayesian models for each P. lacrymatus individual around islands with seabirds (Green) and islands with rats (Yellow). Points are presented alongside best fit lines based on Bayesian model conditional effects, with grey shading indicating 75% quantiles. Bottom: Bayesian posterior densities from hypothesis tests. Posterior probabilities and evidence ratios show the extent to which 1) a positive relationship is supported around islands with seabirds (Left, green), 2) A negative relationship is supported around islands with rats (Middle, yellow), and 3) The relationship between turf algal cover and δ15N is different (that is, more negative) for P. lacrymatus territories around islands with rats compared to around islands with seabirds (Right, yellow).
Extended Data Fig. 3
Extended Data Fig. 3. The influence of P. lacrymatus territory size on aggression around islands with seabirds (Green) and islands with rats (Yellow).
Points represent partialized residuals extracted from Bayesian models for each P. lacrymatus. Best fit lines are extracted from Bayesian model conditional effects, with grey shading indicating 75% quantiles around the mean estimate.
Extended Data Fig. 4
Extended Data Fig. 4. P. lacrymatus density and focal individual total length around islands with seabirds and islands with invasive rats within the Chagos Archipelago.
Each point on the violin plots (left) represents a single P. lacrymatus territory. Mean estimates for conspecific density (A, left) around islands with seabirds (n = 30) and islands with rats (n = 30), and for focal individual total length (B, left) around islands with seabirds (n = 30) and islands with rats (n = 30) are represented by black bars. Posterior densities (Right) in green show the extent to which the following hypotheses are supported.: 1. Conspecific density (A, right) is higher around islands with seabirds and 2. Focal individual total length (B, right) is higher around islands with seabirds. Evidence ratios show how much more likely these hypotheses are supported over the alternative hypotheses. Rat and seabird graphics from PhyloPic.org under Public Domain Dedication 1.0 licenses.
Extended Data Fig. 5
Extended Data Fig. 5. P. lacrymatus conspecific density, nutritional resources, and P. lacrymatus territoriality.
Points represent partialized residuals extracted from Bayesian models for each P. lacrymatus individual around islands with seabirds (Green) and islands with rats (Yellow). Best fit lines are extracted from Bayesian model conditional effects, with grey shading indicating 75% quantiles 75% quantiles around the mean estimate.
Extended Data Fig. 6
Extended Data Fig. 6. P. lacrymatus total length, nutritional resources, and P. lacrymatus territoriality.
Points represent partialized residuals extracted from Bayesian models for each P. lacrymatus individual around islands with seabirds (Green) and islands with rats (Yellow). Best fit lines are extracted from Bayesian model conditional effects, with grey shading indicating 75% quantiles 75% quantiles around the mean estimate.
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