Carryover Effects Drive Competitive Dominance in Spatially Structured Environments

Carryover effects drive competitive dominance in spatially structured environments

Benjamin G. Van Allena,b,1 and Volker H. W. Rudolfb

aDepartment of Biology, Louisiana State University, Baton Rouge, LA 70803; and bDepartment of BioSciences, Rice University, Houston, TX 77005

Edited by Rodolfo Dirzo, Stanford University, Stanford, CA, and approved May 12, 2016 (received for review October 16, 2015) Understanding how changes to the quality of habitat patches affect resource quality, weather, or predation risk) can carry over into new the distribution of species across the whole landscape is critical in our environments by altering the adult traits of individuals, including human-dominated world and changing climate. Although patterns of emigrants (16, 18). These environmentally induced effects operate species’ abundances across a landscape are clearly influenced by dis- through mechanisms, such as plasticity and body condition (18), and persal among habitats and local species interactions, little is known can alter many key life-history traits, including morphology, body size about how the identity and origin of dispersers affect these patterns. and allometry, diet, antipredator defenses, fecundity, or survival (19– Because traits of individuals are altered by experiences in their natal 27). Importantly, such carryover effects can alter individual traits habitat, differences in the natal habitat of dispersers can carry for a lifetime, and persist across multiple generations via maternal/ over when individuals disperse to new habitats and alter their parental effects (28, 29). Such persistent effects challenge the com- fitness and interactions with other species. We manipulated the mon assumption implicit in much theory that individuals simply presence or absence of such carried-over natal habitat effects for up to “reset” traits when dispersing. This assumption may be adequate in eight generations to examine their influence on two interacting species perfectly homogenous environments, because all individuals will across multiple dispersal rates and different habitat compositions. We have carried-over traits that “match” whichever habitat they found that experimentally accounting for the natal habitat of dispersers enter. However, in heterogeneous environments, dispersing indi- significantly influenced competitive outcomes at all spatial scales and viduals frequently encounter a habitat with conditions that differ increased total community biomass within a landscape. However, the from its natal habitat, and phenotypes of dispersing individuals will direction and magnitude of the impact of natal habitat effects was not “match” their current environment because of carryover effects ECOLOGY dependent upon landscape type and dispersal rate. Interestingly, ef- of their natal habitat conditions (30). This mismatch can alter fects of natal habitats increased the difference between species population dynamics (31–34) and interactions with other species performance across the landscape, suggesting that natal habitat (35). For example, snails with antipredator shell morphologies effects could alter competitive interactions to promote spatial coexis- from past predator experiences are vulnerable when they encounter tence. Given that heterogeneity in habitat quality is ubiquitous in nature, environments with new predator types (36). Alternatively, a resource- natal habitat effects are likely important drivers of spatial community rich natal environment for organisms from beetles (34) to birds structure and could promote variation in species performance, which (37) can result in “silver spoon effects” and increase the success may help facilitate spatial coexistence. The results have important impli- of individuals and populations in new environments, even if they cations for conservation and invasive species management. are low quality or mismatching habitats (18, 34, 37). Although increasing evidence suggest that carryover effects are both com- carryover effects | natal habitat effect | competition | metacommunity | mon and important for the structure of natural communities dispersal (15, 16, 35, 38, 39), their interactions with dispersal and variable habitats are not well studied (40). Consequently, how carryover ommunities do not exist in a vacuum; instead, they are effects influence species interactions and distributions across the Cconnected to each other through dispersal of interacting landscape is still poorly understood. species. Consequently, dispersal among different kinds of habitat patches is increasingly recognized as a key factor driving the Significance dynamics and structure of communities from local to regional spatial scales (1–5). In classic models, the persistence and dy- Communities do not exist in a vacuum; instead, they are connected namics of populations within a patch are determined by two fac- to each other through dispersal of interacting species. As a result, tors: the rate of dispersal between patches of habitat and the understanding how changes to the quality of habitat patches species fitness within each local patch (6–8). This view has per- affect communities across the whole landscape is critical in our sisted into metacommunity theory (multiple communities con- human-dominated world and changing climate. When individuals nected by dispersal of individuals between the patches of habitat disperse, they “carry” traits shaped by their natal environment to they occur in) as well, where the influence of dispersers on com- their destinations. Using replicated laboratory landscapes with munity dynamics is generally considered only in terms of their two competing species, we show that these historic effects of natal numbers (i.e., dispersal rate) and habitat-specific performance (1, – habitats have dramatic influences on community structure at all 9 11). Implicit in this case, and for most of spatial ecology, is that spatial scales and multiple dispersal rates. Such historic effects are the interactions and population dynamics within a habitat are ubiquitous in nature, suggesting that changes to local habitat quality solely determined by the quality of that habitat. However, this can have important effects on regional community structure. approach ignores the often substantial variation in individual traits and fitness within and across habitats in a natural system, which Author contributions: B.G.V. and V.H.W.R. designed research; B.G.V. performed research; could alter community dynamics and composition (12–15). B.G.V. analyzed data; and B.G.V. and V.H.W.R. wrote the paper. In metacommunities, one important source of individual varia- The authors declare no conflict of interest. tion arises from “carryover effects,” which can occur when early-life This article is a PNAS Direct Submission. (natal) experience affects later adult traits in a different time or Data deposition: The data reported in this paper have been deposited in the DRYAD place (16, 17). Carryover effects of natal habitat quality present an digital repository, datadryad.org (doi:10.5061/dryad.2gp80). interesting case of individual variation, as by definition their oc- 1To whom correspondence should be addressed. Email: [email protected]. currence is mediated by spatial variation and dispersal (16, 17). For This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. example, conditions experienced in the natal environment (e.g., 1073/pnas.1520536113/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1520536113 PNAS Early Edition | 1of6 Downloaded by guest on October 2, 2021 35, 43). Furthermore, the offspring of beetles who developed in oat flour have prolonged development times and continue to exhibit higher cannibalism/predation rates, indicating transgenerational effect of natal habitat quality (34). As a consequence, populations of both species founded by individuals from wheat flour grow faster to higher population sizes in either habitat, whereas individuals who come from oat are better competitors who are less likely to be excluded by the other species (34, 35). For additional details on how carryover effects alter both species behavior and performance, see refs. 34, 35, and 44.

Experiment. To determine how carryover effects of natal habitat quality influence species distribution across different habitat patches, we factorially manipulated three factors: (i) frequency and spatial arrangement of patches with high- (wheat) vs. low- (oat) habitat quality (i.e., habitat heterogeneity) to create the potential for phenotype-environment mismatch, (ii) dispersal between these patches, and (iii) whether carryover effects matched the natal or new habitat of dispersing individuals. These treatments result in a 2 landscape (HLH and LHL) (Fig. 1) × 3 dispersal treatments (low, 5%, medium, 10%, and high, 40%, of individuals in − each patch emigrate to the adjacent patches month 1) × 2 carryover effects (phenotype matches natal vs. new habitat) factorial design for 12 total treatment groups (Fig. 1). Each landscape had three patches, each consisting of a 7-dram vial with 3.6 g of oat or wheat flour. The two landscape types differed in their configuration of oat (L, low-habitat quality) vs. wheat (H, high-habitat quality) habitat patch, representing a landscape where either patches with high (HLH) or low Fig. 1. Schematic of the experimental set-up of microcosm “landscapes.” (LHL) habitat quality were more frequent (Fig. 1). We replicated the 12 treatments There are two configurations (landscapes) of patches: HLH (high-, low-, then 6 times for 72 independent sets of experimental landscapes with a total of 72 × 3 high-quality habitats) and LHL (low-, high-, then low-quality habitats). Tan patches per landscape = 216 habitat patches. patches indicate wheat flour/high-quality habitat and dark gray patches The six replications of the experimental design were divided into blocks with indicate oat flour/low-quality habitat. Beetles initially started in the patch labeled with their species name, then moved according to dispersal treat- associated stock populations. For each block of treatments, we assigned eight ments (low = 5%, medium = 10%, and high = 40%) in the directions marked stock populations, two oat and two wheat stock colonies per species (which were by the black arrows. To allow or prevent natal habitats from influencing the placed next to their experimental populations in that block), for a total of 48 stock phenotypes of dispersing individuals, we replaced dispersing individuals colonies across the experiment. Stock colonies were maintained as standard from a habitat patch with individuals born in stock colonies with habitat laboratory stocks in 80 g of oat or wheat. Each block of landscapes with associated types that either matched the natal habitat (i.e., phenotypes of dispersers stock colonies was placed into one of three environmental chambers, which were are allowed be influenced by natal habitats) or matched the new habitat kept at 30 °C (±1 °C) and 30% relative humidity (±5%). Details of our experimental (i.e., no carryover effects of natal habitats). Colors of beetles indicate natal methods and the initiation of the experiment can be found in SI Methods.Three habitat-induced phenotypes (i.e., tan beetles developed in wheat flour and dark gray beetles in oat flour). With carryover effects, individuals moving from the microcosm HLH middle patch (for example) would be replaced with individuals born in the middle patch habitat type, oat flour in this case. Without carryover effects, the dispersing individuals would be replaced with individuals born in the destination habitat type, wheat flour in this case.

To identify how carryover effects influence the distribution of interacting species across landscapes with variable habitats, we experimentally manipulated: (i) phenotypes of dispersing individuals to match their natal or new environment, (ii) dispersal rates, and (iii) habitat composition across three habitat patch “landscapes” for two competing flour beetles. We specifically focused on how the presence or absence of natal habitat effects in dispersing individuals carried over to alter competitive dominance, relative abundance, and total abundance of both species at local (patch) and landscape scales. Methods Study Species. We tested how carryover effects influenced the distribution of competing species across multiple habitats using laboratory microcosm “landscapes” populated by two competing species of flour beetle, Tribolium castaneum and Tribolium confusum. The entire life cycle of a flour beetle can take place in milled grain, although beetles can eat many small or soft food items, such as small animal prey, including their own young and the young of other Tribolium species (41). These two species therefore compete largely through intraguild predation in maintained environments (42). The flour type in which beetles develop determines the phenotype of adults, leading to long-lasting habitat-mediated carryover effects. Oat media is a relatively low-quality (nutrient poor) habitat (LHL, low-, high-, then low-quality habitats) for both beetle species, whereas wheat media is the standard high-quality habitat (HLH, high-, low-, then high-quality habitats) for both species. Develop- Fig. 2. Mean abundance (±1SEM)ofT. castaneum (red lines), T. confusum (blue ment in oat flour reduces adult body size, alters adult lifespan, reduces fecundity, lines), and the total of both species abundance (black lines) with or without car- and increases cannibalism/predation rates relative to development in wheat ryover effects of natal habitats in immigrants across landscape configurations with flour (34, 35). Although both species are influenced by the flour type in more low-quality habitat, LHL (A–C) and more high-quality habitat, HLH (D–G)and which they develop, T. castaneum is more negatively affected by low-quality (oat) different dispersal-rate treatments (i.e., proportion of dispersing individuals: low = habitat, but performs better in high-quality (wheat) habitat than T. confusum (34, 5%, mid = 10%, high = 40%). n = 69.

2of6 | www.pnas.org/cgi/doi/10.1073/pnas.1520536113 Van Allen and Rudolf Downloaded by guest on October 2, 2021 Table 1. GLMM results for the effects of allowing natal habitat Results and Discussion quality to influence immigrant traits (Y/N), landscape Total Landscape Abundance. Although the presence of natal habitat configuration (HLH or LHL, see Fig. 1), and dispersal rate (low 5%, effects for dispersers could conceivably have either positive (“silver −1 medium 10%, and high 40% mo ) on the total abundance of spoon”), negative (“mismatch”), or no effects on total abundance both species across whole landscapes across a landscape, we found that they generally increased adult Factor χ2 P densities across species in our experiment (Fig. 2, black lines). Allowing effects of natal habitats on dispersers significantly in- Natal habitat effects (Y/N) 7.59 0.006 creased the total density of adult beetles across landscapes by 9% < Dispersal rate 36.92 0.001 on average, compared with treatments where phenotypes were only < Landscape configuration (HLH or LHL) 252.74 0.001 influenced by their current habitat (Fig. 2 and Table 1). A sub- × < Landscape Dispersal 20.84 0.001 stantial part of this difference occurred because at the highest Natal habitat × Landscape 0.29 0.591 × dispersal rates 31% (169.5 beetles) more adults persisted in land- Natal habitat Dispersal 1.93 0.381 scapes with more high-quality habitat than in the second-most Natal habitat × Landscape × Dispersal 3.49 0.174 × > populous dispersal landscape combination (Fig. 2). This posi- Random effect of block: P 0.05 tive effect of high dispersal rate on total abundance was not Experimental block was included as a random effect, n = 69. Bold entries present in landscapes dominated by low-quality habitat, leading denote significant effects (P < 0.05). to a significant interaction between dispersal rate and landscape type (Fig. 2 and Table 1). Thus, carryover effects from natal habitats generally allowed more adult animals to persist within landscapes of configuration HLH, all in different treatments and blocks, were metacommunities, but this depended on habitat patch configu- lost as a result of experimental error, leaving a total of 69 landscapes for analysis. ration and dispersal rates. We manipulated whether carryover effects matched the natal or new habitat by removing dispersers from their natal habitat patch and replacing them with The positive influence of carryover effects from natal habitats individuals from a stock colony, which either matched the natal or the new on total abundance indicates that their positive effects across spe- habitat. When carryover effects of the natal habitat were allowed to persist cies and habitat transitions outweighed any negative influences of (matched natal habitat), we replaced dispersing individuals with individuals from carryover effects. This pattern likely arises from the fact that high- a stock colony that had the exact same habitat (flour type) as the natal habitat. For quality habitat produces far more offspring in a shorter amount of the treatment preventing carryover effects from natal habitats (i.e., matched new time than low-quality habitat; consequently, more dispersers will ECOLOGY habitat), we used individuals from stock colonies that had the same habitat (flour receive the silver spoon effect of development in high-quality natal type) as the new environment. We used individuals from the same groups of stock habitat, assuming all else is equal. Thus, even if the magnitude of containers for dispersal in both carryover and no-carryover treatments to stan- dardize conditions (i.e., control for any unexpected stock effects). Previous work positive (from high-quality natal habitat) and negative (from low- indicates that natal habitat quality strongly affects beetle traits, but neither quality natal habitat) carryover effects on individual fitness are normal ranges of population density nor experience with other species compa- equal, more individuals will be positively affected by their natal rably alter beetle traits (34, 45). Thus, phenotypes of individuals from stock habitat because of this asymmetrical numerical response. In treat- colonies closely matched phenotypes of individuals in experimental patches. ments that prevented natal habitat effects, individuals moving from This carryover-effect treatment allowed us to test how historic effects of natal high- to low-quality habitat patches immediately assume the phe- habitats on dispersers influenced community dynamics. Specifically, the treat- notype of individuals born in low-quality habitat, which prevents ment in which carryover effects matched the natal environment represents the the beneficial silver spoon effect. In many systems, development correct natural scenario where the condition in the natal habitat of dispersers are allowed to carry over and continue to influence their fitness and interaction in in high-quality habitat increases fecundity, indicating that silver the new environment. The treatment where the natal habitat effects matched spoon effects are common in nature (18, 34, 37, 48). Thus, our results the new environment essentially assumes that the past environment of dispersing individuals has no influence on their current fitness or interactions; that is, individuals immediately “reset” their phenotype to match the new envi- Table 2. GLMM analysis for the effects of allowing natal habitat ronment (which is typically the default assumption of current theory). Thus, any quality to influence immigrant traits (Y/N), landscape significant difference among carryover-effect treatments indicates that we configuration, and dispersal rate on relative abundance of two need to account for the developmental history and natal habitat of dispersers. competing species [T. castaneum density/(T. castaneum + Any significant interactions with habitat configuration treatment (landscape T. confusum densities)] within a landscape across all patches type) or dispersal indicates that these carryover effects are influenced by the 2 dispersal rate and frequency of high- vs. low-quality habitats. Factor χ P

Analysis. Natal habitat effects (Y/N) 6.11 0.013 We used generalized linear mixed models in R [GLMM, package < MASS, function glmmPQL (46, 47)] to determine how carryover effects al- Dispersal rate 38.62 0.001 tered (i) the total abundance (sum of adults of both species) and (ii) species Landscape configuration (HLH or LHL) 5.89 0.015 interactions (i.e., relative abundance of species) across the entire landscape Initial density ratio 21.11 <0.001 (i.e., summed across all three patches) and in a given patch within a landscape, Landscape × Dispersal 2.50 0.286 and how these carryover effects are influenced by landscape configuration and Natal habitat × Landscape 6.40 0.011 dispersal rate. For all tests we only used the densities of adult beetle species Natal habitat × Dispersal 5.25 0.072 recorded during the last time step of the experiment. Dynamics were relatively Natal habitat × Initial density 0.06 0.804 – stable during the last 3 4moinmosttreatmentcombinationsoflandscapes Landscape × Initial density 10.77 0.001 (see Figs. S1 and S2 for full dynamics), so using the last time step is conservative Dispersal × Initial density 1.92 0.382 and ensures that we are examining the long-term effects of our treatments. × × Our GLMM investigating relative abundance at the patch level were performed Natal habitat Landscape Dispersal 5.54 0.063 × × separately for each landscape type because the order of habitat qualities was Landscape Dispersal Initial density 4.66 0.097 opposite in configuration (i.e., the patch habitat-type factor was confounded Natal habitat × Landscape × Initial density 0.42 0.517 with its relative location in the landscape). We used block identity as a random Natal habitat × Dispersal × Initial density 3.36 0.186 effect in all models. Because our response variables were discrete counts of Natal habitat × Landscape × Dispersal × 0.41 0.814 adults or proportions of relative counts of adults, we matched the variance Initial density. structure of our data by using Poisson-distributed error in our model for total Random effect of block: P > 0.05 abundance and binomial-distributed error for our models of relative abundance. To correct for overdispersion of the data, we used quasilikelihood for all tests. A Initial density was used as a covariate to account for stochastic effects, n = 69. more detailed description of our statistical techniques is presented in SI Methods. Bold entries denote significant effects (P < 0.05).

Van Allen and Rudolf PNAS Early Edition | 3of6 Downloaded by guest on October 2, 2021 Table 3. GLMM results for the effects of allowing natal habitat opposite between the two landscape configurations, leading to a quality to influence immigrant traits (Y/N), dispersal rate, and significant interaction among carryover and landscape treatments local patch identity on the relative abundance of two competing (Fig. 2, blue and red lines, and Table 2). When the landscape was species (T. castaneum density/[T. castaneum + T. confusum dominated by high-quality habitat, T. castaneum wasalwaysthe densities]) within each given patch across each microcosm type dominant species and received small benefits from natal habitat Factor χ2 P effects overall (Fig. 2 and Table 2). However, in landscapes where low-quality habitat dominated, allowing natal habitats to carry over Landscape HLH and influence phenotypes of dispersers gave T. confusum alarge Natal habitat effects (Y/N) 1.05 0.305 advantage at low and medium dispersal rates (Fig. 2). At low dis- Dispersal rate 99.25 <0.001 persal rates, allowing carryover effects of natal habitats lead to a Patch 1025.86 <0.001 switch from a landscape slightly dominated by T. castaneum (1.18- Natal habitat × Dispersal 5.61 0.06 times more abundant than T. confusum) to one clearly dominated Natal habitat × Patch 13.12 0.001 by T. confusum (1.81-times more abundant than T. castaneum). At Dispersal × Patch 1568.86 <0.001 medium dispersal rates, allowing carryover effects from natal Natal habitat × Dispersal × Patch 14.26 0.006 habitats more than doubled the dominance of T. confusum relative Random effect of block: P > 0.05 to T. castaneum from 1.61 to 3.88 times. Thus, when low-quality Landscape LHL habitat was more frequent, the presence of carryover effects from Natal habitat effects (Y/N) 6.13 0.013 natal habitats strongly increased the relative competitive domi- Dispersal rate 9.61 0.008 nance of T. confusum (T. confusum 1.7-times more abundant than < Patch 335.09 0.001 T. castaneum across dispersal rates) (Fig. 2). Because T. castaneum × Natal habitat Dispersal 3.88 0.144 always dominated in landscapes with more high-quality habitat, × Natal habitat Patch 11.17 0.0037 carryover effects of natal habitats had to be present for T. confusum × < Dispersal Patch 228.72 0.001 to have any landscape configuration where it was competitively Natal habitat × Dispersal × Patch 26.41 <0.001 > superior. This result is consistent with previous studies that indicate Random effect of block: P 0.05 that changes in natal habitat of dispersers can alter density-dependent n for landscape HLH = 99, for LHL = 108. Bold entries denote significant competitive interactions between these species in new habitats and effects (P < 0.05). help T. confusum to become competitively dominant over T. castaneum (35). Taken together, these results show that when habitats differ among patches, effects of the natal habitats of dispersing individuals suggest that predictions that ignore carryover effects of natal can dramatically alter the relative abundance and dominance of habitats may often underestimate the density of organisms in species across a landscape, but which species benefits depends on metacommunities. dispersal rates and the composition of habitat types across a region.

Effects on Interspecific Competition at the Landscape Scale. In addition Effects on Interspecific Competition at the Local Scale. The presence to increasing total abundance, carryover effects from natal habitats of carryover effects from natal habitats also altered relative species altered competitive outcomes across patches, but the effects were dominance at the local patch level, revealing further patterns that

Fig. 3. Mean abundance (±1SEM)ofT. castaneum (red lines) and T. confusum (blue lines) in each landscape patch with or without carryover effects of natal habitats. T. castaneum starting patches are shaded red, center patches are shaded gray, and T. confusum starting patches are shaded blue. (A–C) LHL-configured landscape results for low (5%), medium (10%), and high (40%) dispersal rates; (D–F) HLH-configured landscape results with the same pattern of dispersal treatments. n = 207 patches inside of 69 independent experimental landscapes.

4of6 | www.pnas.org/cgi/doi/10.1073/pnas.1520536113 Van Allen and Rudolf Downloaded by guest on October 2, 2021 were not always apparent across the whole landscape. Significant dynamics in multiple ways (2, 60, 61). Examples of the influence of higher-order interactions in both models indicate that within-patch carryover effects on natural metacommunity dynamics are begin- dynamics were strongly influenced by the presence or absence of ning to appear (15), but more work is needed to find patterns in the carryover effects from natal habitats (Table 3). For example, frequency and strength of carryover effects in natural communities. when natal habitats were allowed to influence the phenotype of dispersers, this reduced the ability of T. castaneum to invade the Carryover Effects and Spatial Coexistence. Spatial coexistence in T. confusum starting patch in high-quality landscapes. The pro- metacommunities for species that cannot coexist locally is based portion of T. castaneum in their competitors’ starting patch was primarily on trade-offs along habitat-specific fitness and dispersal- on average 45% (low dispersal) and 55% (medium dispersal) related trait axes (1, 9, 11). Carryover effects may represent a novel lower than in treatments where dispersing individuals were not trade-off, because their impacts on relative species performance affected by their natal habitat (i.e., instantly matched the new vary depending on the interplay between the relative abundance of habitat) (Fig. 3 D and E). In contrast, T. confusum invaded the habitat types in the landscape and dispersal rates (35). For exam- T. castaneum starting patch in landscapes with more low-quality ple, each species in this experiment benefited from allowing natal patches much more effectively in the presence of carryover effects habitats to influence phenotypes of immigrants under different from natal habitats, to the point that T. confusum dominated every combinations of dispersal rate and landscape types. These car- patch at medium dispersal rates (Figs. 2 and 3B). Finally, dispersal ryover effects of natal habitats led to T. confusum dominating altered how carryover effects influenced species abundances within across some landscapes, including in high-quality habitat patches, a given patch (Table 3). At low and moderate dispersal rates, car- in which it is usually an inferior competitor (62). When natal ryover effects of natal habitats differed among individual patches habitats were not allowed to influence the phenotypes of immigrants, within a landscape, but at high dispersal rates they had largely the one species alone, T. castaneum, had higher relative abundance same effect regardless of patch identity (Fig. 3 C and F). This pattern across almost all landscapes. Because preventing the effects of can be explained by the fact that high dispersal quickly redistributed natal habitat on disperser phenotype is actually the “unrealistic” individuals and thereby lead to equal distribution of individuals treatment in our experiment, it seems possible that natural systems across all patches (49). Because of this redistribution, carryover may also experience enhanced spatial coexistence as a result of effects were also equally partitioned across individual patches carryover effects. Carryover effects across heterogeneous landscapes and generally benefited both species in a proportionally equal can thus promote variation in relative species performance within

way, especially in landscapes where high habitat quality was more ECOLOGY F a given habitat type and lead to cascading effects across land- frequent (Fig. 3 ). In contrast, when dispersal rates were moderate scapes. Although their effects may be context-dependent, increased to low, individual differences in patch dynamics were possible understanding of carryover effects and their interaction with het- and carryover effects differed across patches. Overall, these re- erogeneous habitat quality may improve ecological forecasting and sults indicate that carryover effects not only altered relative and benefit spatial coexistence theory in natural systems. total abundance of species within a landscape, but also their distribution across individual habitat patches within a landscape. Conclusion Although heterogeneity in habitat quality and dispersal across Carryover Effects in Nature. Studies in more natural field settings landscapes are known to be key drivers of spatial diversity, car- indicate that natal experience can significantly affect individual traits and population dynamics in a variety of taxa [roe deer (50), ryover effects on the traits of dispersing individuals caused by choughs (48), bryozoans (27), parrots (51), bluebirds (15)], suggesting these two factors have been largely neglected (1, 3, 16, 63). Here that patterns similar to our laboratory system are likely across the we show that variation in the natal habitat of dispersing indi- landscape in natural systems. Ecologists, conservationists, and wildlife viduals can lead to carryover effects that significantly influence managers alike should be aware of the quality/type of habitat that landscape and patch-level patterns of the total and relative abun- individuals come from and the possibility of unexpected dynamics in dance of interacting species. Whereas theory and previous experi- focus areas caused by carryover effects of natal habitats on im- ments suggest that carryover effects could alter metacommunity migrating individuals. This aspect highlights a possible difficulty dynamics, this study is, to our knowledge, the first empirical evidence in identifying carryover effects in nature, given that it could be critical of this from a controlled experiment (4, 16, 38). Furthermore, we to know where dispersing individuals come from and what conditions found that carryover effects did not consistently promote the same they experienced to identify potential carryover effects when natal species across landscape and dispersal treatments. Indeed, the pres- and new habitats differ (16, 30, 48, 52, 53). Furthermore, carryover ence of carryover effects magnified differences between species in effects can alter dispersal decisions and capabilities (16, 44). Recent their performance across different landscapes, indicating that they work on condition-dependent dispersal and its implications for could promote variation in species performance and potentially fa- population dynamics is addressing this question already, although cilitate spatial coexistence (10, 11; see ref. 15 for a recent example in there seems to be little focus on multispecies impacts as of yet (44, a natural system). Together, these results demonstrate that we cannot 54–59). In our experiment, we standardized dispersal to isolate accurately predict the dynamics of metacommunities simply based on carryover effects on species interactions. However, there is already the number or rate of dispersers; considering the origin of dispersers clear evidence that carryover effects alter dispersal decisions in this and their traits may be necessary as well. system (44) and exploring the consequences of such changes in dispersal behavior for multispecies dynamics is an important next ACKNOWLEDGMENTS. We thank C. J. Dibble, A. E. Dunham, B. D. Elderd, N. L. Rasmussen, T. E. X. Miller, and two anonymous reviewers for valuable step. Carryover effects can thus alter both the processes of dis- comments and discussion; and C. Tang, J. Lopez, L. LaMere, T. Xu, and V. Kuhn persal between communities and the interactions between species for valuable assistance. This material is based upon work supported by the within communities, suggesting that they can shape metacommunity National Science Foundation under Grants DEB-1311193 and DEB-1256860.

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