Tropical montane and temperate hummingbirds incubate in small installments over long periods

Tropical montane and temperate hummingbirds incubate in small installments over long periods | bioRxiv /* */ /* */ <!-- <!-- /*! * yepnope1.5.4 * (c) WTFPL, GPLv2 */ (function(a,b,c){function d(a){return"[object Function]"==o.call(a)}function e(a){return"string"==typeof a}function f(){}function g(a){return!a||"loaded"==a||"complete"==a||"uninitialized"==a}function h(){var a=p.shift();q=1,a?a.t?m(function(){("c"==a.t?B.injectCss:B.injectJs)(a.s,0,a.a,a.x,a.e,1)},0):(a(),h()):q=0}function i(a,c,d,e,f,i,j){function k(b){if(!o&&g(l.readyState)&&(u.r=o=1,!q&&h(),l.onload=l.onreadystatechange=null,b)){"img"!=a&&m(function(){t.removeChild(l)},50);for(var d in y[c])y[c].hasOwnProperty(d)&&y[c][d].onload()}}var j=j||B.errorTimeout,l=b.createElement(a),o=0,r=0,u={t:d,s:c,e:f,a:i,x:j};1===y[c]&&(r=1,y[c]=[]),"object"==a?l.data=c:(l.src=c,l.type=a),l.width=l.height="0",l.onerror=l.onload=l.onreadystatechange=function(){k.call(this,r)},p.splice(e,0,u),"img"!=a&&(r||2===y[c]?(t.insertBefore(l,s?null:n),m(k,j)):y[c].push(l))}function j(a,b,c,d,f){return q=0,b=b||"j",e(a)?i("c"==b?v:u,a,b,this.i++,c,d,f):(p.splice(this.i++,0,a),1==p.length&&h()),this}function k(){var a=B;return a.loader={load:j,i:0},a}var l=b.documentElement,m=a.setTimeout,n=b.getElementsByTagName("script")[0],o={}.toString,p=[],q=0,r="MozAppearance"in l.style,s=r&&!!b.createRange().compareNode,t=s?l:n.parentNode,l=a.opera&&"[object Opera]"==o.call(a.opera),l=!!b.attachEvent&&!l,u=r?"object":l?"script":"img",v=l?"script":u,w=Array.isArray||function(a){return"[object Array]"==o.call(a)},x=[],y={},z={timeout:function(a,b){return b.length&&(a.timeout=b[0]),a}},A,B;B=function(a){function b(a){var a=a.split("!"),b=x.length,c=a.pop(),d=a.length,c={url:c,origUrl:c,prefixes:a},e,f,g;for(f=0;f<d;f++)g=a[f].split("="),(e=z[g.shift()])&&(c=e(c,g));for(f=0;f<b;f++)c=x[f](c);return c}function g(a,e,f,g,h){var i=b(a),j=i.autoCallback;i.url.split(".").pop().split("?").shift(),i.bypass||(e&&(e=d(e)?e:e[a]||e[g]||e[a.split("/").pop().split("?")[0]]),i.instead?i.instead(a,e,f,g,h):(y[i.url]?i.noexec=!0:y[i.url]=1,f.load(i.url,i.forceCSS||!i.forceJS&&"css"==i.url.split(".").pop().split("?").shift()?"c":c,i.noexec,i.attrs,i.timeout),(d(e)||d(j))&&f.load(function(){k(),e&&e(i.origUrl,h,g),j&&j(i.origUrl,h,g),y[i.url]=2})))}function h(a,b){function c(a,c){if(a){if(e(a))c||(j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}),g(a,j,b,0,h);else if(Object(a)===a)for(n in m=function(){var b=0,c;for(c in a)a.hasOwnProperty(c)&&b++;return b}(),a)a.hasOwnProperty(n)&&(!c&&!--m&&(d(j)?j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}:j[n]=function(a){return function(){var b=[].slice.call(arguments);a&&a.apply(this,b),l()}}(k[n])),g(a[n],j,b,n,h))}else!c&&l()}var h=!!a.test,i=a.load||a.both,j=a.callback||f,k=j,l=a.complete||f,m,n;c(h?a.yep:a.nope,!!i),i&&c(i)}var i,j,l=this.yepnope.loader;if(e(a))g(a,0,l,0);else if(w(a))for(i=0;i (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0];var j=d.createElement(s);var dl=l!='dataLayer'?'&l='+l:'';j.src='//www.googletagmanager.com/gtm.js?id='+i+dl;j.type='text/javascript';j.async=true;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-M677548'); Skip to main content Home About Submit ALERTS / RSS Search for this keyword Advanced Search New Results Tropical montane and temperate hummingbirds incubate in small installments over long periods Justin W. Baldwin , Mario Agustín Loaiza Muñoz , Juliana Sandoval-H , Scott K. Robinson , Ari Martinez , Gustavo Londoño doi: https://doi.org/10.1101/2025.06.19.660382 Justin W. Baldwin 1 University of California Santa Cruz, Ecology and Evolutionary Biology ; Coastal Biology Building 130 MacAllister Way, CA, USA Find this author on Google Scholar Find this author on PubMed Search for this author on this site For correspondence: jubaldwi{at}ucsc.edu galondono{at}icesi.edu.co Mario Agustín Loaiza Muñoz 2 Virginia Tech University, Department of Biological Sciences , 926 West Campus Drive Blacksburg, VA, USA Find this author on Google Scholar Find this author on PubMed Search for this author on this site Juliana Sandoval-H 3 University of Alabama, Alabama Museum of Natural History , 427 6th Ave, Tuscaloosa, AL, USA Find this author on Google Scholar Find this author on PubMed Search for this author on this site Scott K. Robinson 4 University of Florida, Florida Museum of Natural History , 1659 Museum Road Gainesville, FL, USA Find this author on Google Scholar Find this author on PubMed Search for this author on this site Ari Martinez 1 University of California Santa Cruz, Ecology and Evolutionary Biology ; Coastal Biology Building 130 MacAllister Way, CA, USA Find this author on Google Scholar Find this author on PubMed Search for this author on this site Gustavo Londoño 5 Universidad Icesi, Departamento de Biología, Bioprocesos y Biotecnología, Universidad Icesi, Facultad Barberi de Ingeniería, Diseño y Ciencias Aplicadas , Cali AA25608, Colombia Find this author on Google Scholar Find this author on PubMed Search for this author on this site For correspondence: jubaldwi{at}ucsc.edu galondono{at}icesi.edu.co Abstract Full Text Info/History Metrics Supplementary material Data/Code Preview PDF Abstract Life-history strategies and development are shaped by climate and predation. We examined how temperature and nest survival drive incubation behavior in 104 nests of 34 hummingbird species across 2,939m of elevation in the Peruvian and Colombian Andes. At high elevations, cold temperatures led to more frequent, brief incubation bouts and extended incubation periods; survival modulated incubation behavior with no effect on development. Hummingbirds had the highest egg surface-area to volume ratios among all birds; in 147 species, incubation periods increased with decreasing ambient temperatures. We propose a new hypothesis to explain how in cold conditions, heat transfer to the embryo is fragmented into smaller increments and therefore extended over longer periods, underscoring the role of adult behavior in mediating embryonic temperature mismatches and life-history tradeoffs. Introduction Why some animals reach maturity in days while others take years is a fundamental question in ecology and evolution ( 1 , 2 ). Developmental duration, a key dimension of life history ( 3 ), is shaped by mechanistic and physiological constraints ( 4 – 6 ), phylogeny ( 7 ), environmental conditions and survival rates ( 8 , 9 ). In birds, the incubation period is an energetically expensive phase of development ( 10 , 11 ) during which adults balance competing demands. Adults must ensure that egg temperatures remain high and stable (∼34-40.5° C, well above “physiological zero” of 26° C ( 12 – 15 )). Species with uniparental care, however, must leave the nest to refuel; during this time, developing embryos are subjected to cold and variable temperatures and incur fitness costs ( 16 ). Harsh conditions, rain and food scarcity can extend parental absences and decrease egg temperatures ( 15 , 17 ) factors that slows development ( 16 , 18 ). Exacerbating these challenges, the threat of nest predation forces adults to conceal ( 19 ) or limit nest visits ( 20 , 21 ), and selects for accelerated development ( 3 , 4 ). When predation pressure is relaxed, incubation behavior changes ( 22 ) and development is prolonged ( 23 , 24 ). Nevertheless, the relative importance of abiotic conditions and nest survival rates on incubation and life history remains uncertain ( 9 ). Our understanding of the tradeoff between abiotic and biotic constraints on incubation results is limited for several reasons. Tropical birds are widely thought to have uniformly low rates of nest attendance ( 17 , 18 , 25 ), but incubation behavior from many tropical species remains unknown ( 26 ). Additionally, temperate-tropical comparisons often use nest attentiveness, the fraction of daytime that birds spend incubating on the nest ( 12 , 25 ), but this metric alone might be insufficient: diurnal incubation can be fragmented into many short or few long bouts, maintaining nest attentiveness (Fig. S1) but also likely impacting egg temperatures ( 16 ) and predation risk ( 20 ). Montane hummingbirds in the Neotropics offer a unique opportunity to disentangle the joint effects of environmental conditions and nest predation on incubation behavior and life-history traits. Hummingbirds are extremely sensitive to changes in environmental temperatures because powered hovering flight consumes large amounts of energy ( 27 , 28 ), and much of the resulting heat produced is lost to the immediate environment due to the birds’ small size and high ratio of surface-area to volume ( 29 , 30 ). The different temperature regimes they encounter as they breed from sea-level to above 4,000m may affect their range of body size (1.9–20.2g), incubation period (12–23 days) and egg mass (0.25–1.75g) ( 6 , 31 – 34 ). Moreover, some major traits that explain life-history variation across birds ( 34 ) are controlled for in hummingbirds: all are nectarivorous and have 2-egg clutches, uniparental care and similar nest architecture ( 34 ). Embryonic development might be especially sensitive to environmental temperatures and highly dependent on parental incubation, because their small eggs rapidly lose heat when unattended ( 35 ). In this study we examined how nest survival rates and environmental temperatures influence the incubation and development of 34 species of Neotropical hummingbirds, using observations from 293 complete days of incubation in104 nests, spanning 2,939 m of elevation in the Peruvian and Colombian Andes. We hypothesize that hummingbirds are uniquely temperature-sensitive due to high ratios of egg surface-area to volume and therefore employ locally adaptive incubation strategies across the elevational gradient. Accordingly, hummingbirds at cold, high elevations should employ more frequent, brief incubation bouts compared to species at warm, low elevations ( 9 , 15 , 36 ). Moreover, long incubation recesses, which expose embryos to cold temperatures that slow development ( 16 , 37 ), are likely compensated for by extended incubation periods and increased egg mass, following the “embryonic temperature hypothesis” ( 18 ). Additionally, we explored how elevational variation in nest survival rates ( 38 ) shapes both incubation behavior ( 20 ) and incubation periods using estimates of nest survival from 390 nests of the same 34 species. We test these predictions with comparisons of incubation behavior, incubation periods, egg mass and egg shape using our new data from the field and data from the literature ( 6 , 39 – 41 ). Results and Discussion Hummingbird incubation behavior in the Andes We used in situ dataloggers and thermocouples inserted into active nests ( Fig. 1A ) to determine incubation behavior from 104 nests of 34 species of hummingbirds during eight years of fieldwork at eight field sites in Peru and Colombia ( Fig. 1B-D ) ( 42 ). We obtained a mean of 2.82 full days of incubation per nest (SD = 1.46, range 1-16 days, 293 days total). Incubation behavior varied within and across species and along the elevational gradient ( Fig. 1E ): in high-elevation species (e.g., Metallura tyrianthina) incubation bouts were frequent (mean = 82.6 trips/day, range: 49-183) and brief (mean = 11.3 min, range: 4.8-14.7), but in comparison, in low-elevation species (e.g. Glaucis hirsutus) incubation bouts were fewer (mean = 25.1 trips/day, range: 15-39) and extended (mean = 40.3 min, range: 11.6-69.3). Download figure Open in new tab Fig. 1. Incubation behavior of montane hummingbirds in Colombia and Peru along an elevational gradient. ( A ) Active nests were monitored using remotely deployed data loggers with thermocouples inserted below eggs to collect nest (red) and ambient temperatures (blue). Temperature traces revealed incubation bouts (grey) and recesses (black; here an Amethyst-throated Sunangel, Heliangelus amethysticollis ). ( B ) Eight years of fieldwork across 2,939 meters of elevation in the Andes spread across four field sites in Colombia ( C ) and Peru each ( D yielded 293 full days of incubation behavior from 104 nests of 34 species ( E ). Horizontal thin grey lines separate days from same species. Grey rectangles show incubation bouts and black rectangles show incubation recesses. (E) Days of incubation are ordered by species and daily ambient temperature, with station (B-D) mean diurnal ambient temperatures visualized according to the same color scale. Photos of well-sampled species provided by Lina Peña Ramirez, Carlos Calle and contributors to Wikimedia Commons (see acknowledgments) under Creative Commons licenses. Icon (A) made by Isabella Burgos. Basemaps (B-D) from Stadia/OpenStreetmap. Ambient temperatures shape hummingbird incubation behavior and life history Hummingbird eggs likely lose heat faster than other species, due to their small size and uniquely cylindrical (“tic-tac”) shape. We predicted that the ratio of egg surface-area to volume is higher in hummingbirds than in other birds. In a comprehensive sample of egg dimensions ( 41 ), hummingbirds had the highest ratio of egg surface-area to volume among birds worldwide (Trochilidae; mean = 2.27, SE = 0.025, N = 12): 3.8 times higher than the average family (thrushes, Turdidae; mean = 0.59, SE = 0.03, N = 36), and ∼89 times higher than the family with the lowest surface-area to volume ratio (ostriches: Struthionidae; mean = 0.026, N = 1; Fig. 2A ). Accordingly, we posit that hummingbird eggs are highly temperature-sensitive and dependent on adult incubation behavior. Download figure Open in new tab Fig. 2. Thermally sensitive hummingbird eggs demand temperature-dependent incubation strategies; these in turn shape development. ( A) Hummingbirds have the largest ratios of egg surface-area to volume across all bird families (Trochilidae mean = 2.27, SE = 0.025, N = 12). Icons indicate mean egg surface-area to volume for ostriches (mean = 0.0256) and thrushes (mean = 0.593, SE = 0.003, N = 36). High levels of incubation fragmentation are characterized by many incubation trips ( B ), brief incubation bouts ( C ) and brief incubation recesses ( D ) – all traits on x-axis were natural-log transformed. Phylogenetic generalized linear mixed models reveals that temperature affects incubation fragmentation and interacts with body mass ( E ). Small-bodied ( FG ) and large-bodied species ( HI ) are shown from high and low elevations, respectively. Decreases in nest temperature were driven by nonlinear effects of incubation recess duration as well as interactions with ambient temperature and clutch mass ( JK ). Small eggs in cold temperatures experienced the largest decrease in temperature, dropping 4 degrees in 7.6 minutes, whereas larger eggs dropped 4 degrees in 13.1 minutes to (thin grey lines - K). ( L ) Phylogenetic regressions show prolonged incubation periods in cold temperatures in 147 species worldwide (estimate = -0.041, SE = 0.010, T = -4.303, p< 0.001, red line) and in 13 species on the elevational gradient (estimate = -1.234, SE = 0.527, t = -2.323, p = 0.039, black line, colored diamonds correspond to species in F-I). We thank Felix Uribe and Charles J. Sharp for providing photos on Wikimedia Commons under Creative Commons licenses as well as Carlos Calle for the photo of Phlogophilus . Silhouettes in A from PhyloPic and we thank Charles J. Sharp for providing photos on Wikimedia Commons under Creative Commons licenses. Across the elevational gradient, the daily number of incubation bouts and recesses, as well as their duration, were interdependent, so we used principal component analyses to define an aggregate metric, hereafter “incubation fragmentation” (Table S1). This approach allowed us to separate days of incubation behavior with few long incubation bouts from days of incubation behavior fragmented into many, brief bouts ( Fig. 2B-D ). Phylogenetic generalized linear mixed models of incubation fragmentation revealed a strong significant effect of ambient temperature (posterior mean = -0.486, 95% credible interval: -0.657 – -0.314, Table S2, Fig. 2E ). But when temperatures rose, incubation fragmentation decreased more in large species than in small species (temperature x mean body mass interaction, posterior mean = -0.166, 95% credible interval: -0.322 – -0.006, Table S2, Fig. 2F-I ). Incubation fragmentation was unrelated to traditional measures of nest attentiveness (Pearson’s correlation coefficient = -0.015, t = -0.254, df = 275, p-value = 0.800, Fig. S2), and analysis of nest attentiveness (instead of incubation fragmentation) revealed no influence of temperature (Table S3). Our results were robust to including phylogenetic relatedness in the construction of principal components (Table S4) and phylogenetic uncertainty (Table S5). Although during incubation recesses, nest temperatures eventually approximated ambient temperatures (Fig. S3), nests with small eggs lost temperature faster – but only when ambient temperatures were cold (three-way interaction between non-linear effect of incubation recess duration, ambient temperature and clutch mass: F 5737,1 = 81.902, p-value < 0.0001, Table S6). During warm ambient temperatures, clutch mass conferred no thermal advantage ( Fig. 2J ). In contrast, during cold temperatures (10°C), large clutch mass buffered temperature loss: for example, a species with 2g clutch mass lost 4°C of nest temperature during a 13.1-minute incubation recess, whereas a species with 1g clutch mass lost the same amount in 7.6 minutes ( Fig. 2K ). As body mass and egg mass scale allometrically ( 43 ), the interacting effects of temperature and body mass on incubation behavior ( Fig. 2E ) could be explained by the way large-bodied birds with correspondingly large eggs (these have low egg surface-area to volume ratios; Fig. 2A ) can decrease incubation fragmentation (and extend the duration of their incubation recesses) without exposing their embryos to low temperatures. Our results were similar when accounting for phylogenetic and temporal non-independence, although the support for some parameters decreased (Table S7, Fig. S4). Across the elevational gradient, development accelerated with increasing local ambient temperatures: the incubation period decreased from 22 days at 10.7°C (2,879m) to 16 days at 22.9°C (431m) (univariate phylogenetic regression: estimate = -1.234, SE = 0.527, t = -2.323, p = 0.039, N = 13; Fig. 2L diamonds, black line). Across the western hemisphere, hummingbirds in colder areas also had significantly longer incubation periods than those in warm areas (temperature estimate = -0.041, SE = 0.010, t = -4.303, p < 0.001, N = 147, Table 1 , Fig. 2L black points, red line). Previous studies have found inconsistent relationships between nest attendance and incubation period ( 12 , 25 ) and species with long incubation recesses have long incubation periods ( 12 , 18 ). However, our results suggest that in cold ambient temperatures, incubation recesses are short whereas incubation periods are long. This is additionally surprising as temperature has no influence on incubation periods across all birds ( 6 ). We also recovered the expected allometry ( 5 , 6 ) between incubation period and body mass ( Table 1 ). Temperature had no effect on egg mass (estimate = -0.025, SE = 0.020, t = -1.212, p = 0.217, N = 104, Table S8). However, we found a weak, yet marginally significant positive relationship between egg mass and incubation period, after accounting for body mass (estimate = 0.112, SE = 0.060, t = 1.878, p = 0.064, N = 89, Table S9, Fig. S5), which suggests that increased parental investment in egg mass is reflected in extended incubation periods ( 18 ). This correlation is surprising, as egg mass and size are likely under strong physical constraints in hummingbirds ( 44 ). Our inferences were robust to phylogenetic uncertainty (Table S10). View this table: View inline View popup Download powerpoint Table 1. Temperature, body mass and insularity influence hummingbird incubation periods. Phylogenetic generalized linear models of incubation periods. Significant parameters in bold. ⍰ Denotes terms eliminated during model selection. Adjusted R 2 =0.235 and λ = 0.221 in final model. Nest survival shapes hummingbird incubation and life history We additionally obtained estimates of nest survival rates from 390 nests of 34 species by exploring 6,092 cumulative days of nest observations; during this time we registered 178 instances of predation. When data were pooled across the gradient and within stations, aggregated Mayfield estimators ( 45 ) of daily survival rates were high ( Fig. 3A , gradient: 0.957, SE = 0.003, N = 390 nests; range: Pantiacolla : 0.948, SE = 0.005, N = 170, Tatamá: 0.967, SE = 0.006, N = 47; Table S11) - higher than other cup-nesting species and near the highest values of cavity-nesters ( 39 ). Predation rates were low ( Fig. 3B , Table S11). To correlate survival with incubation behavior, we modelled daily nest-level survival and predation rates using phylogenetic logistic exposure models ( 46 ). Shared ancestry (i.e., phylogenetically pooled random intercepts) explained substantial variation ( Figs. 3CD , Fig. S12). In contrast, neither nest height (posterior mean = 0.07, 95% credible interval: -0.79 – 0.87), elevation (posterior mean = 0.03, 95% credible interval: -0.37 – 0.44) nor interannual variation significantly affected daily survival rates ( Fig. 3E-G , Table S12). Daily predation rates were likewise unaffected by ecological variables (Table S13, Fig. S6). Daily survival rates had a significant positive effect on incubation fragmentation (posterior mean = 0.144, 95% credible interval: -0.266 – -0.019; Fig. 3H , Table S2), suggesting that when nest survival is low, visits to the nest were less frequent and lasted longer. These findings support a longstanding idea that predation risk influences incubation behavior ( 20 ). Our regression analyses were robust to the use of predation rates instead of survival rates (Table S14). Download figure Open in new tab Fig. 3. Nest survival rates of montane hummingbirds vary with phylogeny, and influence incubation behavior but not development. Mayfield estimators of daily survival ( A ) and predation rates ( B ) along the elevational gradient where N denotes number of nests. Horizontal dotted lines denote pooled estimates across gradient. ( C ) Phylogenetic logistic exposure models reveal notable variation in daily survival rates across species, with weak species-specific effects of nest height. Vertical dashed lines indicate zero. Tip color denotes species-average survival estimate of predicted values for each nest (C). ( D-G ) Points show species-specific posterior means, and horizontal lines show 95% credible intervals of effect sizes from phylogenetic logistic exposure models, with significant effect sizes in red. Shaded rectangles show hyperparameter distributions for random intercepts (D) and random slopes of nest height (E). Effects of interannual variation (F) and elevation (G) applied to all species equally. Across the elevational gradient, incubation fragmentation increased with increasing daily rates of nest survival ( H ). Survival rates had no effect on incubation periods ( I , estimate = 0.009, SE = 0.029, T = 0.327, p = 0.750, N = 30, horizontal lines denote standard errors). Island-dwelling hummingbirds have significantly longer incubation periods than continental species ( J , estimate = 0.097, SE = 0.031, T = 3.171, p = 0.0019, red lines show means). Given that low survival caused birds to spend longer incubation bouts on the nest (keeping egg temperatures high), we predicted that eggs in such nests would develop faster, in line with life-history theory ( 3 , 23 ), and because long incubation bouts could keep egg temperatures high ( 18 ). To test the influence of nest survival on incubation period, we performed a regression analysis on the 30 species of hummingbirds for which both daily survival rates and incubation periods are available ( 39 ). These results revealed no effect of survival rates on incubation periods (estimate = 0.009, SE = 0.029, t = 0.327, p = 0.750, N = 30, Table S15, Fig. 3I ) and instead confirmed the significant effect of ambient temperature (Table S15). These conclusions were robust to measurement error in survival estimates (Table S16). In addition, insular species had on average 1.1-day longer incubation periods than continental species (estimate = 0.097, SE = 0.031, t = 3.171, p = 0.002, N = 147, Table 1 , Fig. 3J ). Although this effect size is small, it corroborates the “slow pace of life” on islands ( 6 , 23 , 47 , 48 ). Overall, while nest survival rate does influence incubation behavior in hummingbirds, its effect on their life-history traits seems weaker than that of ambient temperature, although more data are needed. This relatively small effect of variation in survival rate on nesting behavior contrasts with patterns in other tropical families ( 21 , 49 ). We suspect that hummingbirds might be uniquely unaffected by nest predators because of their allometrically unparalleled flight speeds ( 50 ), pugnaciousness ( 51 ) and ability to nest in enemy-free areas ( 52 ). Additionally, predators prefer large eggs ( 53 ), which offer more protein: in context, a nest predator in the Peruvian highlands would consume the same egg mass from a single Andean Guan egg (Penelope montagnii, 73.4g, N = 1), as from ∼7 Great Thrush eggs (Turdus fuscater, mean = 10.5g, SE = 0.114, N = 86) or ∼146 Tyrian Metaltail eggs (Metallura tyrianthina, mean = 0.504g, SE = 0.014, N = 49; Fig. S7). The Incubation Fragmentation Hypothesis Our results add a novel thermal perspective to hummingbird life history and reveal extreme, unexpectedly variable incubation behavior in the Neotropics in a single avian family. Along the elevational gradient, colder temperatures fragmented incubation behavior ( Fig. 1E , Fig. 2B-I ). Likewise, global temperature variation affected incubation fragmentation in a sample of 201 species from 37 families ( 36 ) (phylogenetic regression: estimate = -0.146, SE = 0.037, t-value = -3.950, p = 0.00001, λ = 0.989, N = 201; Fig. S8), suggesting a universal effect of temperature on incubation behavior. Our finding -- that across the globe hummingbirds in cold temperatures (where incubation recesses are frequent and brief) require extended incubation periods ( Fig. 2DL , Table 1 ) – is then particularly surprising, as the “embryonic temperature hypothesis” (hereafter ETH) predicts that species with protracted incubation recesses should have extended incubation periods ( Fig. 4A ) due to cold exposure during extended parental absences ( 12 , 18 ). Download figure Open in new tab Fig. 4. The Incubation Fragmentation Hypothesis. ( A ) The IFH and ETH make different predictions about the relationship between incubation recess duration and incubation period, possibly due to the differently-shaped relationships ( B ) between temperature and embryonic developmental efficiency. (B–ETH curve adapted from ( 15 )). ( C-F ) Asymptotic warming during incubation bouts reveals nest temperatures approaching target temperatures for species with high and low incubation fragmentation (C,E). Target temperature (dashed grey line) is 5% below asymptote estimates from Gompertz functions (red lines) fitted to nest temperatures during diurnal incubation bouts. (D,F) Nest temperature traces are colored by distance from target temperatures; ambient temperatures shown in pale blue line. ( G ) Nest temperatures of species with high incubation fragmentation (blue diamond in A) are less frequently above target incubation temperatures on a daily basis compared to nest temperatures of species with low incubation fragmentation (yellow diamond in A). Species with high levels of incubation fragmentation take longer to complete the incubation period (A). To explain our results, we propose an alternative hypothesis, the “incubation fragmentation hypothesis” (IFH). Under both hypotheses, endothermic adult birds provide close physical contact with eggs during incubation, rapidly transferring heat to their ectothermic embryos. Embryonic temperature influences growth efficiency ( 54 ), which is highest at incubation temperatures near adult body temperatures (34–40.5°C ( 12 – 15 )). The hypotheses differ in how embryonic growth efficiency decreases when temperatures drop below this range ( Fig. 4B ). Citing poultry science ( 14 ), the ETH assumes convex decay of growth efficiency with decreasing egg temperature ( 15 , 18 ). But as embryonic temperature thresholds and thermal sensitivity vary strongly across species ( 13 ), we propose that growth efficiency might decay asymptotically in hummingbirds ( Fig. 4B ). Even if hummingbirds also show convex decay, their high surface-area to volume ratios could rapidly drop embryo temperatures below target incubation temperatures soon after incubating adults leave the nest ( Fig. 1A , Fig. 4CD , Fig. S9), particularly impacting small species in cold environments ( Fig. 2JK ). Additionally, frequent interruptions of incubation might stunt any developmentally essential processes that are initiated only after sustained exposure to target incubation temperatures (i.e. duration-dependent regulation ( 55 , 56 ); Fig. S10). Consequently, species with high ( Fig. 4CD ) and low rates of incubation fragmentation ( Fig. 4EF ) develop differently: frequent, short incubation recesses decrease the total time an embryo spends at developmentally relevant incubation temperatures ( Fig. 4G , lower daily “cooking time” ( 16 , 57 )); extended incubation periods compensate for the lower daily thermal dose ( Fig. 4A , 2EL ) and increased egg mass (Fig. S5) as in ( 18 ). Whereas the ETH highlights reduced embryonic growth during incubation recesses, the IFH emphasizes increased embryonic growth during long incubation bouts. However, as number and duration of incubation recess and of incubation bouts are interdependent ( Fig. 2B-D ), this difference in emphasis produces conflicting predictions about the effect of behavior on development ( Fig. 4A ). Although we were unable to formally test the ETH without hummingbird egg temperature measurements across all elevations, we evaluated two corollary predictions. Provided ambient temperatures are well below egg temperatures ( 18 ), long incubation recesses alone can reduce egg temperatures and delay development ( 12 ), supporting the ETH. We could not readily measure hummingbird egg temperatures due to their size, so we used a limited sample of two nests. All nest and egg temperatures in these nests were significantly correlated (all ρ > 0.6, p < 0.001; Fig. S11), and target egg temperatures exceeded 28° – well above local mean ambient diurnal temperatures (< 20.2° C). In other words, the predictions of the ETH were expected ( Fig. 4A ). Moreover, variation in target egg temperature across elevations might explain differences in incubation period ( 12 ), and body temperature limits target egg temperature. Yet in over 877 hours of internal body temperatures from 112 non-torpid hummingbirds (24 species, from 520-2,500m in Colombia ( 58 )), nocturnal body temperatures did not vary across elevation (mean = 37.07° C, range = 30.02-41.05; phylogenetic mixed model: elevation effect = 0.21, SE = 0.52, 95% CI = 0.10-2.08, Table S17, Fig. S12). Therefore, we infer that target egg temperatures during incubation neither vary across elevation nor explain variation in incubation periods in hummingbirds. Avian life-history research remains an active area of research; our results suggest that our understanding of these processes will improve greatly as we acquire more data using new technologies for poorly known tropical species ( 26 ). With our new data on the duration and frequency of incubation bouts, we can now understand how parental behavior affects multiple life-history tradeoffs in response to both abiotic (temperature) and biotic (predation) conditions ( 59 ). Mismatches between optimal and realized developmental temperatures during incubation can incur myriad costs such as increased mortality, decreased developmental speed ( 60 ), reduced immunocompetence ( 61 ), altered locomotor performance ( 62 ) and increased fearfulness ( 63 ). As global temperatures continue to change, such mismatches might become more frequent and could influence species survival and population persistence. Overall, our results speak to wide-ranging effects of avian parental behavior that have the potential to shape evolutionary processes via life-history tradeoffs, particularly when behavioral strategies buffer organisms from their environment ( 64 , 65 ). Funding National Science Foundation grant DEB-1120682 (GAL) Association of Field Ornithologists, Alexander Skutch Award (GAL) Wilson Ornithological Society, Louis Agassiz Fuertes Award (GAL) American Ornithologists’ Union, Alexander Wetmore Award (GAL) Fulbright, Student Research Scholarship (JWB) Author contributions Writing – review & editing: JWB, SKR, AM, GAL Competing interests Authors declare that they have no competing interests. Data and materials availability All data and code are available on Zenodo (DOI: 10.5281/zenodo.15670484, https://zenodo.org/records/15670485 ) and detailed methods are in the Supplemental Materials. Supplementary Materials Materials and Methods Supplementary Text Figs. S1 to S12 Tables S1 to S17 References ( 66 – 102 ) Acknowledgments We thank everyone who supported these experiments; see supplementary materials for a full list. Funder Information Declared National Science Foundation, https://ror.org/021nxhr62 , DEB-1120682 Association of Field Ornithologists, https://ror.org/05g27v878 , Alexander Skutch Award Wilson Ornithological Society, https://ror.org/03cqty937 , Louis Agassiz Fuertes Award American Ornithologists Union , Alexander Wetmore Award Fulbright Association, https://ror.org/00300j256 , Student Research Scholarship Footnotes https://zenodo.org/records/15670485 References and Notes 1. ↵ S. C. Stearns , The Evolution Of Life Histories ( Oxford University PressOxford , 1998 ). 2. ↵ P. D. Boersma , “Why some birds take so long to hatch” ( 1982 ). 3. ↵ D. Lack , Ecological Adaptations for Breeding in Birds ( Methuen, London , 1968 ). 4. ↵ R. E. Ricklefs , An analysis of nesting mortality in birds . Smithson Contrib Zool , 1 – 48 ( 1969 ). 5. ↵ R. E. Ricklefs , Patterns of Growth in BIrds . Ibis 110 , 419 – 451 ( 1968 ). OpenUrl CrossRef 6. ↵ C. R. Cooney , C. Sheard , A. D. Clark , S. D. Healy , A. Liker , S. E. Street , C. A. Troisi , G. H. Thomas , T. Székely , N. Hemmings , A. E. Wright , Ecology and allometry predict the evolution of avian developmental durations . Nat Commun 11 ( 2020 ). 7. ↵ D. C. Deeming , G. F. Birchard , R. Crafer , P. E. Eady , Egg mass and incubation period allometry in birds and reptiles: Effects of phylogeny . J Zool 270 , 209 – 218 ( 2006 ). OpenUrl CrossRef Web of Science 8. ↵ V. Remeš , T. E. Martin , Environmental influences on the evolution of growth and developmental rates in passerines . Evolution (N Y) 56 , 2505 – 2518 ( 2002 ). OpenUrl 9. ↵ C. J. Conway , T. E. Martin , Evolution of passerine incubation behavior: influence of food, temperature, and nest predation . Evolution 54 , 670 – 685 ( 2000 ). OpenUrl CrossRef PubMed Web of Science 10. ↵ J. B. Williams , “ Energetics of Avian Incubation ” in Avian Energetics and Nutritional Ecology ( Springer US, Boston, MA , 1996 ; http://link.springer.com/10.1007/978-1-4613-0425-8_11 ), pp. 375 – 415 . 11. ↵ J. M. Reid , P. Monaghan , G. D. Ruxton , “Resource allocation between reproductive phases: the importance of thermal conditions in determining the cost of incubation” ( 2000 ); https://royalsocietypublishing.org/ . 12. ↵ T. E. Martin , S. K. Auer , R. D. Bassar , A. M. Niklison , P. Lloyd , Geographic variation in avian incubation periods and parental influences on embryonic temperature . Evolution (N Y) 61 , 2558 – 2569 ( 2007 ). OpenUrl CrossRef 13. ↵ D. R. Webb , Thermal tolerance of avian embryos: a review . Condor 89 , 874 – 898 ( 1987 ). OpenUrl CrossRef 14. ↵ H. Lundy , A review of the effects of temperature, humidity, turning and gaseous environment in the incubator on the hatchability of the hen’s egg . The Fertility and Hatchability of Hen’s Egg ( 1969 ). 15. ↵ C. J. Conway , T. E. Martin , Effects of ambient temperature on avian incubation behaviour . Behavioural Ecology 11 , 178 – 188 ( 2000 ). OpenUrl CrossRef Web of Science 16. ↵ C. R. Olson , C. M. Vleck , D. Vleck , Periodic cooling of bird eggs reduces embryonic growth efficiency . Physiological and Biochemical Zoology 79 , 927 – 936 ( 2006 ). OpenUrl CrossRef PubMed Web of Science 17. ↵ A. D. Chalfoun , T. E. Martin , Latitudinal variation in avian incubation attentiveness and a test of the food limitation hypothesis . Anim Behav 73 , 579 – 585 ( 2007 ). OpenUrl CrossRef Web of Science 18. ↵ T. E. Martin , “Egg size variation among tropical and temperate songbirds: An embryonic temperature hypothesis” ( 2008 ); www.pnas.orgcgidoi10.1073pnas.0709366105 . 19. ↵ K. B. Ekanayake , M. A. Weston , D. G. Nimmo , G. S. Maguire , J. A. Endler , C. Küpper , The bright incubate at night: Sexual dichromatism and adaptive incubation division in an open-nesting shorebird . Proceedings of the Royal Society B: Biological Sciences 282 ( 2015 ). 20. ↵ A. F. Skutch ., Do Tropical Birds Rear As Many Young As They Can Nourish? Ibis 91 , 430 – 455 ( 1949 ). OpenUrl CrossRef 21. ↵ N. Şahin Arslan , T. E. Martin , Visual predators and diurnal nest predation provide support for the Skutch Hypothesis and explain evolved incubation behaviors in a montane tropical bird community . Ornithology 141 ( 2024 ). 22. ↵ J. J. Fontaine , T. E. Martin , Parent birds assess nest predation risk and adjust their reproductive strategies . Ecol Lett 9 , 428 – 434 ( 2006 ). OpenUrl CrossRef PubMed Web of Science 23. ↵ C. Bosque , M. T. Bosque , Nest predation as a selective factor in the evolution of developmental rates in altricial birds . American Naturalist 145 , 234 – 260 ( 1995 ). OpenUrl CrossRef Web of Science 24. ↵ F. Sayol , P. A. Downing , A. N. Iwaniuk , J. Maspons , D. Sol , Predictable evolution towards larger brains in birds colonizing oceanic islands . Nat Commun 9 ( 2018 ). 25. ↵ B. I. Tieleman , J. B. Williams , R. E. Ricklefs , Nest attentiveness and egg temperature do not explain the variation in incubation periods in tropical birds . Funct Ecol 18 , 571 – 577 ( 2004 ). OpenUrl CrossRef 26. ↵ A. C. Lees , K. V. Rosenberg , V. Ruiz-Gutierrez , S. Marsden , T. S. Schulenberg , A. D. Rodewald , A roadmap to identifying and filling shortfalls in Neotropical ornithology . Auk 137 , 1 – 17 ( 2021 ). OpenUrl 27. ↵ A. Shankar , D. R. Powers , L. M. Dávalos , C. H. Graham , The allometry of daily energy expenditure in hummingbirds: An energy budget approach . Journal of Animal Ecology 89 , 1254 – 1261 ( 2020 ). OpenUrl CrossRef PubMed 28. ↵ R. K. Suarez , Hummingbird flight: Sustaining the highest mass-specific metabolic rates among vertebrates . Experientia 48 , 565 – 570 ( 1992 ). OpenUrl CrossRef PubMed Web of Science 29. ↵ A. Shankar , C. H. Graham , J. R. Canepa , S. M. Wethington , D. R. Powers , Hummingbirds budget energy flexibly in response to changing resources . Funct Ecol 33 , 1904 – 1916 ( 2019 ). OpenUrl CrossRef 30. ↵ C. Bergmann , Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Größe . Göttinger Studien 1 , 595 – 708 ( 1847 ). OpenUrl 31. ↵ C. H. Graham , J. L. Parra , C. Rahbek , J. A. McGuire , Phylogenetic structure in tropical hummingbird communities . Proc Natl Acad Sci U S A 106 , 19673 – 19678 ( 2009 ). OpenUrl Abstract / FREE Full Text 32. O.E. Murillo-García , M. E. De La Vega , K. Pérez-Castillo , “Elevation does not strongly influence interspecific variation in body size of small Tropical endotherms” ( 2020 ). 33. W. A. Calder III . , “ Characteristics and constraints of incubation in hummingbirds ” in Avian Incubation (Oxford University PressOxford , 2001 ; https://academic.oup.com/book/54355/chapter/422515051 ), pp. 207–222. 34. ↵ K. L. Schuchmann , “ Family Trochilidae (Hummingbirds )” in Handbook of the Birds of the World, Vol. 5: Barn-Owls to Hummingbirds ( Lynx Editions, Barcelona , 1999 ) vol. 5 , pp. 468 – 680 . OpenUrl 35. ↵ J. E. Lizarazo , “ ¿Cómo afectan las condiciones ambientales las propiedades térmicas del sistema huevo-nido en aves? ,” thesis, Universidad Icesi, Cali, Colombia ( 2018 ). 36. ↵ T. Jin , Q. Hu , Y. Liu , J. Li , S. Pan , J. Xu , Latitudinal variations in incubation behaviour among uniparental incubating birds . Journal of Animal Ecology , doi: 10.1111/1365-2656.70022 ( 2025 ). OpenUrl CrossRef 37. ↵ C. M. Vleck , “Energetic Cost of Incubation in the Zebra Finch” ( 1981 ); https://www.jstor.org/stable/1367313?seq=1&cid=pdf-. 38. ↵ G. A. Londoño , J. P. Gomez , M.A. Sánchez-Martínez , D. J. Levey , S. K. Robinson , Changing patterns of nest predation and predator communities along a tropical elevation gradient . John Wiley and Sons Inc [Preprint] ( 2023 ). doi: 10.1111/ele.14189 . OpenUrl CrossRef PubMed 39. ↵ Z. F. Smart , P. A. Downing , S. H. Austin , H. F. Greeney , G. A. Londoño , M. I. Nahid , W. D. Robinson , C. Riehl , Ecology and life history predict avian nest success in the global tropics . Proc Natl Acad Sci U S A 121 ( 2024 ). 40. S. M. Billerman , B. K. Keeney , P. G. Rodewald , T. S. Schulenberg D. W. Winkler , S. M. Billerman , I. J. Lovette , “ Hummingbirds (Trochilidae )” in Birds of the World , S. M. Billerman , B. K. Keeney , P. G. Rodewald , T. S. Schulenberg , Eds. ( Cornell Lab of Ornithology , 2024 ). 41. ↵ M. C. Stoddard , E. H. Yong , D. Akkaynak , C. Sheard , J. A. Tobias , L. Mahadevan , Avian egg shape: Form, function, and evolution . Science (1979) 356 , 1249 – 1254 ( 2017 ). OpenUrl Abstract / FREE Full Text 42. ↵ G. A. Londoño , J. P. Gomez , M.A. Sánchez Martínez , D. J. Levey , S. K. Robinson , Changing patterns of nest predation and predator communities along a tropical elevation gradient . Ecol Lett 26 , 609 – 620 ( 2023 ). OpenUrl CrossRef PubMed 43. ↵ J. Y. Juang , P. Y. Chen , D. C. Yang , S. P. Wu , A. Yen , H. I. Hsieh , The avian egg exhibits general allometric invariances in mechanical design . Sci Rep 7 ( 2017 ). 44. ↵ R. Montgomerie , J. E. Thompson , T. R. Birkhead , The Shapes of Birds’ Eggs: Evolutionary Constraints and Adaptations . Am Nat 6 , E215 – E231 ( 2021 ). OpenUrl 45. ↵ D. H. Johnson , Estimating Nest Success: The Mayfield Method and an Alternative . Auk 96 , 651 – 661 ( 1979 ). OpenUrl 46. ↵ T. L. Shaffer , A Unified Approach to Analyzing Nest Success . Auk 121 , 526 – 540 ( 2004 ). OpenUrl CrossRef 47. ↵ R. Covas , Evolution of reproductive life histories in island birds worldwide . Proceedings of the Royal Society B: Biological Sciences 279 , 1531 – 1537 ( 2012 ). OpenUrl CrossRef PubMed 48. ↵ Y. Xiong , R. Rozzi , Y. Zhang , L. Fan , J. Zhao , D. Li , Y. Yao , H. Xiao , J. Liu , X. Zeng , H. Xu , Y. Jiang , F. Lei , Convergent evolution toward a slow pace of life predisposes insular endotherms to anthropogenic extinctions . Sci Adv 10 , 8240 ( 2024 ). OpenUrl CrossRef 49. ↵ C. K. Ghalambor , T. E. Martin , Comparative manipulation of predation risk in incubating birds reveals variability in the plasticity of responses . Behavioral Ecology 13 , 101 – 108 ( 2002 ). OpenUrl CrossRef Web of Science 50. ↵ C. J. Clark , Courtship dives of Anna’s hummingbird offer insights into flight performance limits . Proceedings of the Royal Society B: Biological Sciences 276 , 3047 – 3052 ( 2009 ). OpenUrl CrossRef PubMed Web of Science 51. ↵ A. Rico-Guevara , M. Araya-Salas , Bills as daggers? A test for sexually dimorphic weapons in a lekking hummingbird . Behavioral Ecology 26 , 21 – 29 ( 2015 ). OpenUrl CrossRef 52. ↵ H. F. Greeney , M. R. Meneses , C. E. Hamilton , E. Lichter-Marck , R. W. Mannan , N. Snyder , H. Snyder , S. M. Wethington , L. A. Dyer , Trait-mediated trophic cascade creates enemy-free space for nesting hummingbirds . Sci Adv 1 ( 2015 ). 53. ↵ M. S. Vazquez , M.A. Rodríguez-Cabal , D. V. Gonzalez , G. S. Pacheco , G. C. Amico , Different nest predator guild associated with egg size in the Patagonian temperate forest . Bird Study 65 , 478 – 483 ( 2018 ). OpenUrl CrossRef 54. ↵ J. F. Gillooly , J. H. Brown , G. B. West , V. M. Savage , E. L. Charnov , Effects of size and temperature on metabolic rate . Science (1979) 293 , 2248 – 2251 ( 2001 ). OpenUrl Abstract / FREE Full Text 55. ↵ S. Teague , G. Primavera , B. Chen , Z. Y. Liu , L. A. Yao , E. Freeburne , H. Khan , K. Jo , C. Johnson , I. Heemskerk , Time-integrated BMP signaling determines fate in a stem cell model for early human development . Nat Commun 15 ( 2024 ). 56. ↵ S. Tozer , G. L. Dréau , E. Marti , J. Briscoe , Temporal control of BMP signalling determines neuronal subtype identity in the dorsal neural tube . Development (Cambridge) 140 , 1467 – 1474 ( 2013 ). OpenUrl Abstract / FREE Full Text 57. ↵ J. F. Gillooly , S. I. Dodson , The relationship of neonate mass and incubation temperature to embryonic development time in a range of animal taxa . J Zool 251 , 369 – 375 ( 2000 ). OpenUrl CrossRef 58. ↵ D. C. Revelo Hernández , J. W. Baldwin , G. A. Londoño , Ecological drivers and consequences of torpor in Andean hummingbirds . Proceedings of the Royal Society B: Biological Sciences 290 ( 2023 ). 59. ↵ T. E. Martin , Avian Life-History Evolution has an Eminent Past: Does it Have a Bright Future? Auk 121 , 289 – 301 ( 2004 ). OpenUrl CrossRef 60. ↵ S. E. Durant , W. A. Hopkins , G. R. Hepp , J. R. Walters , Ecological, evolutionary, and conservation implications of incubation temperature-dependent phenotypes in birds . Biological Reviews 88 , 499 – 509 ( 2013 ). OpenUrl CrossRef 61. ↵ S. E. DuRant , W. A. Hopkins , D. M. Hawley , G. R. Hepp , Incubation temperature affects multiple measures of immunocompetence in young wood ducks (Aix sponsa) . Biol Lett 8 , 108 – 111 ( 2012 ). OpenUrl CrossRef PubMed 62. ↵ B. C. Hopkins , S. E. Durant , G. R. Hepp , W. A. Hopkins , Incubation temperature influences locomotor performance in young wood ducks (Aix sponsa) . J Exp Zool A Ecol Genet Physiol 315 A, 274–279 ( 2011 ). 63. ↵ A. Bertin , L. Calandreau , M. Meurisse , M. Georgelin , R. Palme , S. Lumineau , C. Houdelier , A. S. Darmaillacq , L. Dickel , V. Colson , F. Cornilleau , C. Rat , J. Delaveau , C. Arnould , Incubation temperature affects the expression of young precocial birds’ fear-related behaviours and neuroendocrine correlates . Sci Rep 8 ( 2018 ). 64. ↵ D. W. Pfennig K. C. Chenard , R. A. Duckworth , “ The Special Case of Behavioral Plasticity? ” in Phenotypic Plasticity & Evolution , D. W. Pfennig , Ed. ( CRC Press, Boca Raton, ed. 1 , 2021 ) vol. 1 , pp. 301 – 326 . OpenUrl 65. ↵ J. M. Baldwin , A New Factor in Evolution . American Naturalist 30 , 441 – 451 ( 1896 ). OpenUrl CrossRef View the discussion thread. Back to top Previous Next Posted June 25, 2025. Download PDF Supplementary Material Data/Code Email Thank you for your interest in spreading the word about bioRxiv. NOTE: Your email address is requested solely to identify you as the sender of this article. Your Email * Your Name * Send To * Enter multiple addresses on separate lines or separate them with commas. You are going to email the following Tropical montane and temperate hummingbirds incubate in small installments over long periods Message Subject (Your Name) has forwarded a page to you from bioRxiv Message Body (Your Name) thought you would like to see this page from the bioRxiv website. Your Personal Message CAPTCHA This question is for testing whether or not you are a human visitor and to prevent automated spam submissions. Share Tropical montane and temperate hummingbirds incubate in small installments over long periods Justin W. Baldwin , Mario Agustín Loaiza Muñoz , Juliana Sandoval-H , Scott K. Robinson , Ari Martinez , Gustavo Londoño bioRxiv 2025.06.19.660382; doi: https://doi.org/10.1101/2025.06.19.660382 Share This Article: Copy Citation Tools Tropical montane and temperate hummingbirds incubate in small installments over long periods Justin W. Baldwin , Mario Agustín Loaiza Muñoz , Juliana Sandoval-H , Scott K. Robinson , Ari Martinez , Gustavo Londoño bioRxiv 2025.06.19.660382; doi: https://doi.org/10.1101/2025.06.19.660382 Citation Manager Formats BibTeX Bookends EasyBib EndNote (tagged) EndNote 8 (xml) Medlars Mendeley Papers RefWorks Tagged Ref Manager RIS Zotero Tweet Widget Facebook Like Google Plus One Subject Area Ecology Subject Areas All Articles Animal Behavior and Cognition (7640) Biochemistry (17706) Bioengineering (13902) Bioinformatics (41978) Biophysics (21465) Cancer Biology (18611) Cell Biology (25528) Clinical Trials (138) Developmental Biology (13387) Ecology (19920) Epidemiology (2067) Evolutionary Biology (24332) Genetics (15615) Genomics (22519) Immunology (17747) Microbiology (40424) Molecular Biology (17194) Neuroscience (88662) Paleontology (667) Pathology (2838) Pharmacology and Toxicology (4827) Physiology (7650) Plant Biology (15160) Scientific Communication and Education (2046) Synthetic Biology (4302) Systems Biology (9826) Zoology (2271)