Mixed company: a framework for understanding the composition and organization of mixed-species animal groups

Abstract

Mixed-species animal groups (MSGs) are widely acknowledged to increase predator avoidance and foraging efficiency, among other benefits, and thereby increase participants' fitness. Diversity in MSG composition ranges from two to 70 species of very similar or completely different phenotypes. Yet consistency in organization is also observable in that one or a few species usually have disproportionate importance for MSG formation and/or maintenance. We propose a two-dimensional framework for understanding this diversity and consistency, concentrating on the types of interactions possible between two individuals, usually of different species. One axis represents the similarity of benefit types traded between the individuals, while the second axis expresses asymmetry in the relative amount of benefits/costs accrued. Considering benefit types, one extreme represents the case of single-species groups wherein all individuals obtain the same supplementary, group-size-related benefits, and the other extreme comprises associations of very different, but complementary species (e.g. one partner creates access to food while the other provides vigilance). The relevance of social information and the matching of activities (e.g. speed of movement) are highest for relationships on the supplementary side of this axis, but so is competition; relationships between species will occur at points along this gradient where the benefits outweigh the costs. Considering benefit amounts given or received, extreme asymmetry occurs when one species is exclusively a benefit provider and the other a benefit user. Within this parameter space, some MSG systems are constrained to one kind of interaction, such as shoals of fish of similar species or leader-follower interactions in fish and other taxa. Other MSGs, such as terrestrial bird flocks, can simultaneously include a variety of supplementary and complementary interactions. We review the benefits that species obtain across the diversity of MSG types, and argue that the degree and nature of asymmetry between benefit providers and users should be measured and not just assumed. We then discuss evolutionary shifts in MSG types, focusing on drivers towards similarity in group composition, and selection on benefit providers to enhance the benefits they can receive from other species. Finally, we conclude by considering how individual and collective behaviour in MSGs may influence both the structure and processes of communities.

Keywords: co-evolution; evolution of sociality; interspecific communication; keystone species; mimicry; mutualism; public information; species networks.

Figure 1

A framework to classify interactions between pairs of individuals in single‐species groups (SSGs) and mixed‐species groups (MSGs). The x axis represents asymmetry in the nature of the benefits traded between the partners, ranging from similar, supplementary benefits (S, light red), to highly complementary ones (C, dark blue). The y axis represents the division in the total amount of the benefits transferred between the partners, ranging from providers and users benefitting equally (E), to them sharing asymmetrically (U), with the user benefitting more. The x axis is categorical, with different (D, medium purple) benefits being intermediary between S and C and providing continuity across the categorical axis; the y axis is quantitative and continuous (from 50:50 benefit division to 100:0).

Figure 2

Examples of mixed‐species group (MSG) types, plotted in the parameter space of Fig. 1. For simplicity, each point is here an interaction between species. Different interactions within the same MSG are connected with a line and are of the same colour. In some MSG systems, all relationships are confined to a part of the parameter space, whereas in others, different kinds of relationships can be included in the same MSG. Yellow: an MSG of surgeonfish (Acanthurus leucosternon and A. auranticavus), matched in size and shape, although not colour. Orange: dash dot goatfish (Parupeneus barberinus, provider) and checkerboard wrasse (Halichores hortulanus, user), associations. Green: a mixed‐species bird flock, including highly dissimilar kinds of interactions – (i) provider: orange‐billed babbler (Turdoides rufescens, OBBA); (ii) sentinel species: greater racket‐tailed drongo (Dicrurus paradiseus, GRTD); (iii) fly‐catching user: Malabar trogon (Harpactes fasciatus, MATR); (iv) gleaning user: white‐faced starling (Sturnornis albofrontatus, WFST). Photographs of surgeonfish by Rucha Karkarey, and goatfish‐wrasse by Anne Theo. Photographs of OBBA (Iain Robson), GTDR (Lip Kee Yap), and MATR (Vinay Bhat) from Wikimedia Commons, and that of WFST by Eben Goodale.

Figure 3

Drivers that may underlie changes between mixed‐species group (MSG) types over evolutionary time. A: providers may evolve so that their share of benefits are more equitable with their associates in MSGs, if such changes are possible. An example of a complex co‐evolved system is shown between meerkats (Suricata suricatta), and fork‐tailed drongos (Dicrurus adsimilis) (Flower et al., 2014; photograph by Tom Flower). B, species that regularly interact in MSGs may become more similar to other members, so that the ‘oddity effect’ is less severe and so that their activities (e.g. movement speed) are better matched. An example of potential mimicry in fish is shown in which yellow goatfish (Mulloidichthys martinicus, in dotted circle) joins a group of tomtate grunt (Maemulon aurolineatum) (Pereira et al., 2011; photograph by the authors, published under a Creative Commons license).