Open… access code peer review

 

Affiliations: 1) Max Planck Institute for Evolutionary Anthropology, 2) University of California Santa Barbara, 3) University of Rochester. *Corresponding author:

 

This preregistration has been pre-study peer reviewed and received an In Principle Recommendation by:

Esther Sebastián González (2020) The role of behavior and habitat availability on species geographic expansion. Peer Community in Ecology, 100062. 10.24072/pci.ecology.100062. Reviewers: Caroline Nieberding, Tim Parker, and Pizza Ka Yee Chow

Cite as: Logan CJ, McCune KB, Chen N, Lukas D. 2020. Implementing a rapid geographic range expansion - the role of behavior and habitat changes (http://corinalogan.com/Preregistrations/gxpopbehaviorhabitat.html) In principle acceptance by PCI Ecology of the version on 16 Dec 2021 https://github.com/corinalogan/grackles/blob/0fb956040a34986902a384a1d8355de65010effd/Files/Preregistrations/gxpopbehaviorhabitat.Rmd.

See the easy-to-read HTML version and the reproducible manuscript (Rmd) version for the code

 

ABSTRACT

It is generally thought that behavioral flexibility, the ability to change behavior when circumstances change, plays an important role in the ability of a species to rapidly expand their geographic range (Chow et al., 2016; Griffin & Guez, 2014; e.g. Lefebvre et al., 1997; Sol et al., 2002, 2005, 2007; Sol & Lefebvre, 2000). However, it is an alternative non-exclusive possibility that an increase in the amount of available habitat can also facilitate a range expansion (Hanski & Gilpin, 1991; Wiens, 1997). Great-tailed grackles (Quiscalus mexicanus) are a social, polygamous species that is rapidly expanding its geographic range (Wehtje, 2003) and eats a variety of human foods in addition to foraging on insects and on the ground for other natural food items (K. Johnson & Peer, 2001). They are behaviorally flexible (Logan, 2016a) and highly associated with human-modified environments (K. Johnson & Peer, 2001), thus offering an opportunity to assess the role of behavior and habitat change over the course of their expansion. We first aim to compare behavior in wild-caught grackles from three populations across their range (core of the original range, a more recent population in the middle of the northern expansion front, a very recent population on the northern edge of the expansion front) to investigate whether: 1) certain behaviors (flexibility, innovativeness, exploration, and persistence) have higher averages and variances in some populations relative to others, and 2) individuals in a more recently established population exhibit more dispersal behavior (i.e., individuals are more likely to move away from their parents). Secondly, we aim to investigate whether habitat availability, not necessarily inherent species differences, can explain why great-tailed grackles are able to much more rapidly expand their range than their closest relative, boat-tailed grackles (Q. major) (Post et al., 1996; Wehtje, 2003). We will examine temporal habitat changes over the past few decades using existing databases on presence/absence of both grackle species and compare habitat variables to determine whether: 3) these species use different habitats, habitat suitability and connectivity (which combined determines whether habitat is available) has increased across their range, and what proportion of suitable habitat both species occupy. Finally, we will 4) determine whether changes in behavioral traits facilitate the rapid GTGR expansion by comparing their behavior with BTGR on the same tests in aim 1. Results will elucidate whether the rapid geographic range expansion of great-tailed grackles is associated with individuals differentially expressing particular behaviors and/or whether the expansion is facilitated by the alignment of their natural behaviors with an increase in suitable habitat (i.e., human-modified environments).

INTRODUCTION

It is generally thought that behavioral flexibility, the ability to change behavior when circumstances change (see Mikhalevich et al., 2017 for theoretical background on our flexibility definition), plays an important role in the ability of a species to rapidly expand their geographic range (Chow et al., 2016; Griffin & Guez, 2014; e.g., Lefebvre et al., 1997; Sol et al., 2002, 2005, 2007; Sol & Lefebvre, 2000). These ideas predict that flexibility, exploration, and innovation facilitate the expansion of individuals into completely new areas and that their role diminishes after a certain number of generations (Wright et al., 2010). In support of this, experimental studies have shown that latent abilities are primarily expressed in a time of need (A. M. Auersperg et al., 2012; Bird & Emery, 2009; Laumer et al., 2018; Manrique & Call, 2011; e.g., Taylor et al., 2007). Therefore, we do not expect the founding individuals who initially dispersed out of their original range to have unique behavioral characteristics that are passed on to their offspring. Instead, we expect that the actual act of continuing a range expansion relies on flexibility, exploration, innovation, and persistence, and that these behaviors are therefore expressed more on the edge of the expansion range where there have not been many generations to accumulate relevant knowledge about the environment.

It is also possible that a recent increase in the amount of available habitat can facilitate a geographic range expansion (Hanski & Gilpin, 1991; Wiens, 1997). A species may not need to be behaviorally flexible to move into new areas if they can continue to use the same types of habitat they are accustomed to. Human-modified environments are increasing (Goldewijk, 2001; e.g., Liu et al., 2020; Wu et al., 2011), and species associated with these habitats show differences in their behavior (Chejanovski et al., 2017; e.g., Ciani, 1986; Federspiel et al., 2017). These species offer an opportunity for simultaneous investigation of the roles of behavior and increased habitat availability for a rapidly increasing geographic range expansion.

To determine whether behavior is involved in a rapid geographic range expansion, direct measures of individual behavioral abilities must be collected in populations across the range of the species (see the discussion on the danger of proxies of flexibility in Logan et al., 2018). We plan to test whether behavioral flexibility and/or an increase in habitat availability play a role in the rapid geographic range expansion of great-tailed grackles (Quiscalus mexicanus). Great-tailed grackles are behaviorally flexible (Logan, 2016a), rapidly expanding their geographic range (Wehtje, 2003), and highly associated with human-modified environments (K. Johnson & Peer, 2001), thus offering an opportunity to assess the role of behavior and habitat change over the course of their expansion. This social, polygamous species eats a variety of human foods in addition to foraging on insects and on the ground for other natural food items (K. Johnson & Peer, 2001). This feature increases the ecological relevance of comparative cognition experiments that measure individual behavior abilities: grackles eat at outdoor cafes, from garbage cans, and they eat our crops. As such, they generally gain experience in the wild with approaching and opening novel objects to seek food (e.g., attempting to open a ketchup packet at an outdoor cafe, climbing into garbage cans to get french fries at the zoo, dunking sugar packets in water), which makes the tests involving human-made apparatuses ecologically relevant for this species.

We first aim to compare behavior in wild-caught great-tailed grackles from three populations across their range (core of the original range: Central America, a more recent population in the middle of the northern expansion front: Arizona, a very recent population on the northern edge of the expansion front: California). We will investigate whether certain behaviors have higher averages and variances in the edge population relative to older populations. Specifically, we will investigate behavioral flexibility measured as reversal learning of food-filled colored tube preferences (Logan, 2016b; Logan et al., 2019), innovativeness measured as the number of loci they solve to access food on a puzzlebox (A. M. I. Auersperg et al., 2011; Logan et al., 2019), exploration measured as the latency to approach a novel object in the absence of nearby food (McCune KB et al., 2019; Mettke-Hofmann et al., 2009), and persistence measured as the proportion of sessions they participated in during the flexibility and innovativeness experiments. We will also examine whether individuals in a recently established population (California) are more likely to move away from the location they hatched by determining whether their average relatedness (calculated using single nucleotide polymorphisms, SNPs) is lower than what we would expect if individuals move randomly (Sevchik et al., 2019).

Second, we aim to investigate whether habitat availability, not necessarily inherent species differences, explains why great-tailed grackles are able to much more rapidly expand their range than their closest relative, boat-tailed grackles (Q. major) (Post et al., 1996; Wehtje, 2003). Detailed reports on the breeding ecology of these two species indicate that range expansion in boat- but not great-tailed grackles may be constrained by the availability of suitable nesting sites (Selander & Giller, 1961; Wehtje, 2003). Boat-tailed grackles nest primarily in coastal marshes, whereas great-tailed grackles nest in a variety of locations (e.g., palm trees, bamboo stalks, riparian vegetation, pines, oaks). However, this apparent difference in habitat breadth has yet to be rigorously quantified. Great-tailed grackles inhabit a wide variety of habitats (but not forests) at a variety of elevations (0-2134m), while remaining near water bodies, while boat-tailed grackles exist mainly in coastal areas (Selander & Giller, 1961). Both species have similar foraging habits: they are generalists and forage in a variety of substrates on a variety of different food items (Selander & Giller, 1961). We will use ecological niche modeling to examine temporal habitat changes over the past few decades using observation data for both grackle species from existing citizen science databases. We will compare this data with existing data on a variety of habitat variables. We identified suitable habitat variables from Selander & Giller (1961), K. Johnson & Peer (2001), and Post et al. (1996) (e.g., types of suitable land cover including marine coastal, wetlands, arable land, grassland, mangrove, urban), and we added additional variables relevant to our hypotheses (e.g., distance to nearest uninhabited suitable habitat patch to the north, presence/absence of water in the area). A suitable habitat map will be generated across the Americas using ecological niche models. This will allow us to determine whether the range of great-tailed grackles, but not boat-tailed grackles, might have increased because their habitat suitability and connectivity (which combined determines whether habitat is available) has increased, or whether great-tailed grackles now occupy a larger proportion of habitat that was previously available.

Third, we aim to compare behavior in one population of wild-caught boat-tailed grackles with that of great-tailed grackles on the same tests in aim 1 (behavioral flexibility, innovativeness, exploration, and persistence, but not dispersal). Similar to great-tailed grackles, boat-tailed grackles are social and polygamous, and eat human foods (Post, 1992; Post et al., 1996), which increases the ecological relevance of these tests. Determining whether great-tailed grackles perform better on these tests would provide support for the hypothesis that their behavior could be causing their rapid geographic range expansion. Alternatively, if boat-tailed and great-tailed grackles perform similarly, this would suggest that environmental, rather than behavioral, variables may play a larger role in restricting the boat-tailed grackle range expansion.

There could be multiple mechanisms underpinning the results we find, however our aim is to narrow down the role of changes in behavior and changes in habitats in the range expansion of great-tailed grackles. Results will elucidate whether the rapid geographic range expansion of great-tailed grackles is associated with individuals differentially expressing particular behaviors and/or whether the expansion is facilitated by the alignment of their natural behaviors with an increase in suitable habitat (i.e., human-modified environments).

A. STATE OF THE DATA

This preregistration was written (Mar 2020) prior to collecting any data from the edge and core populations, therefore we were blind to these data. However, we were not blind to some of the data from the Arizona population: some of the relatedness data (SNPs used for Hypothesis 2 to quantify relatedness to infer whether individuals disperse away from relatives) from the middle population (Arizona) has already been analyzed for other purposes (n=57 individuals, see Sevchik et al. (2019)). Therefore, it will be considered secondary data: data that are in the process of being collected for other investigations. We have now collected blood samples from many more grackles in Arizona, therefore we will redo the analyses from the Arizona population in the analyses involved in the current preregistration. In May 2020, we completed data collection for other variables at the Arizona field site: flexibility and innovation (Logan et al., 2019), and exploration (McCune KB et al., 2019), and we will soon analyze this data, therefore it will also be considered secondary data. This preregistration was submitted in May 2020 to PCI Ecology for pre-study peer review. We received the reviews, and revised and resubmitted in Aug 2020, and it passed pre-study peer review in Oct 2020.

Level of data blindness: Logan and McCune collect the behavioral data (Q1) and therefore have seen this data for the Arizona population. Lukas has access to the Arizona data and has seen some of the summaries in presentations. Chen has not seen any data.

B. PARTITIONING THE RESULTS

We may decide to present the results from different hypotheses in separate articles. We may also decide to test these hypotheses in additional species.

C. RESEARCH QUESTIONS

Q1 (4 behaviors: great-tailed grackles): Are there differences in behavioral traits (flexibility, innovation, exploration, and persistence) between populations across the great-tailed grackle’s geographic range? (Fig. 1 & 2).

Prediction 1: If behavior modifications are needed to adapt to new locations, then there will be a higher average and/or larger variance of at least some traits thought to be involved in range expansions (behavioral flexibility: speed at reversing a previously learned color preference based on it being associated with a food reward; innovativeness: number of options solved on a puzzle box; exploration: latency to approach/touch a novel object; and persistence: proportion of trials participated in with higher numbers indicating a more persistent individual) in the grackles sampled from the more recently established population relative to the individuals sampled in the older populations (Table 1). Higher averages in behavioral traits indicate that each individual can exhibit more of that trait (e.g., they are more flexible/innovative/exploratory/persistent). Perhaps in newly established populations, individuals need to learn about and innovate new foraging techniques or find new food sources. Perhaps grackles require flexibility to visit these resources according to their temporal availability and the individual’s food preferences. Perhaps solving such problems requires more exploration and persistence. Higher variances in behavioral traits indicate that there is a larger diversity of individuals in the population, which means that there is a higher chance that at least some individuals in the population could innovate foraging techniques and be more flexible, exploratory, and persistent, which could be learned by conspecifics and/or future generations. This would support the hypothesis that changes in behavioral traits facilitate the great-tailed grackle’s geographic range expansion.

Prediction 1 alternative 1: Human-modified environments are suitable habitat for grackles (e.g., Selander & Giller (1961), K. Johnson & Peer (2001), Wehtje (2003)), and the amount of human-modified environments has increased and is increasing (e.g., Liu et al. (2020)). If the original behaviors exhibited by this species happen to be suited to the uniformity of human-modified landscapes (e.g., urban, agricultural, etc. environments are modified in similar ways across Central and North America), then the averages and/or variances of these traits will be similar in the grackles sampled from populations across their range (Table 1). This supports the hypothesis that, because this species is closely associated with human-modified environments, which may be similar across the geographic range of this species, individuals in new areas may not need to learn very much about their new environment: they can eat familiar foods and access these foods in similar ways across their range (e.g., fast food restaurant chains likely make the same food and package it in the same packaging in Central and North America, outdoor cafes and garbage cans also look the same across their range). Alternatively, it is possible that 2.9 generations at the edge site is too long after their original establishment date to detect differences in the averages and/or variances (though evidence from experimental evolution suggests that, even after 30 generations there is no change in certain behaviors when comparing domestic guinea pigs with 30 generations of wild-caught captive guinea pigs Künzl et al. (2003), whereas artificial selection can induce changes in spatial ability in as little as two generations Kotrschal et al. (2013)). If the sampled individuals had already been living at this location for long enough (or for their whole lives) to have learned what they need about this particular environment (e.g., there may no longer be evidence of increased flexibility/innovativeness/exploration/persistence), there may be no reason to maintain population diversity in these traits to continue to learn about this environment. We will not be able to distinguish between these two alternatives within alternative 1 because populations closer to the northern edge of this species’ range were too small for us to establish such a field site. Both of these alternatives assume that learning is costly (e.g., Mery & Kawecki, 2005), therefore individuals avoid it if they can. In the first case, individuals might not need to rely much on learning because they are attending to familiar cues across their range, therefore they only need to learn where in this new space space these cues are located. In the second case, individual learning that the founding individuals needed to rely on to move into this new space could have been lost due to potential pressure to reduce this investment as soon as possible after moving to a new location.

Figure 1. What is the role of behavior in a rapid range expansion? The great-tailed grackle study sites are indicated by the colored circles: edge (yellow; California), middle (red; Arizona), and core (white; Central America) and correspond with those in Figure 3.