The Great-tailed grackle (Quiscalus mexicanus) is a polygamous bird species that is originating from Central America and rapidly expanding its geographic range toward the North, and in which females were long thought to be the sole nest builders and caretakers of the young. In their pre-registration [1], Folsom and collaborators report repeated occurrences of male parental care and develop hypotheses aiming at better understanding the occurrence and the fitness consequences of this very rarely observed male behavior. They propose to assess if male parental care correlates with the circulating levels of several relevant hormones, increases offspring survival, is a local adaptation, and is a mating strategy, in surveying three populations located in Arizona (middle of the geographic range expansion), California (northern edge of the geographic range), and in Central America (core of the range). This study is part of a 5-year bigger project.
Both reviewers and I strongly value Folsom and collaborators’ commitment to program a study, in natural field conditions, of a rare, yet likely evolutionary-important behavior, namely parental care by males of the great-tailed grackle. Yet, we all also recognized that it is a risky endeavor, and as a consequence, we wondered about the authors’ ability to reach a sufficient sample size to statistically test (all) hypotheses and predictions with enough confidence (e.g. risk of type I errors, also known as false positives).
Folsom and collaborators acknowledged these limitations in their pre-registration. (i) They made the exploratory nature of their research work clear to readers. (ii) They adapted their analysis plan in running prior power analyses and in focusing on effect sizes (estimates and confidence intervals). (iii) Last and not least, Folsom and collaborators clearly exposed a priori hypotheses, their associated predictions and alternatives, and ranked the latter based on their plausibility according to knowledge in the current and other study systems. Developing theory about male parental care behavior more generally with regard to a polygamous species that is rapidly expanding its geographic range and that is considered not to provide male parental care is without any doubt an added value to this study.
In summary, while this study will likely be insufficient to fully understand male parental care behavior of great-tailed grackles, it is much needed because it will definitely allow rejecting some predictions (e.g., if this behavior is present in all the studied populations, it would be common across range against expectation; finding only one male providing care to an unrelated offspring would lead to reject the prediction that males only care for their own offspring) and thus it will help laying the foundation of future research directions.
I strongly support the pre-registration system and thank all the contributors for producing a fruitful discussion throughout the review process, which in fine improved the clarity and logic of this pre-registration. Given the positive and encouraging reviews, the detailed and thorough answers to all comments by Folsom and collaborators, and their satisfactory and interesting revisions, I am happy to recommend this pre-registration and I look forward to seeing its outcomes.

References

[1] Folsom MA, MacPherson M, Lukas D, McCune KB, Bergeron L, Bond A, Blackwell A, Rowney C, Logan CJ. 2020. Investigating the rare behavior of male parental care in great-tailed grackles. corinalogan.com/Preregistrations/gmalecare.html In principle acceptance by PCI Ecology of the version on 15 June 2020 corinalogan/grackles/blob/master/Files/Preregistrations/gmalecare.Rmd.

Agriculture in the XXI century faces the huge challenge of having to provide food to a rapidly growing human population, which is expected to reach 10.9 billion in 2100 (UUNN 2019), by means of practices and methods that guarantee crop sustainability, human health safety, and respect to the environment (UUNN 2015). Such regulation by the United Nations ultimately entails that agricultural scientists are urged to design strategies and methods that effectively minimize the use of harmful chemical products to control pest populations and to improve soil quality.
One of the most, if not the most, sustainable, safe, and environmentally friendly approach to apply against pests is Biological Pest Control (BPC, hereafter), that is, the use of natural enemies to control the populations of pest organisms. The concept of BPC is by no means new: long back to the 300 AC, Chinese farmers built bamboo bridges between citrus trees to facilitate the foraging of the ant species Oecophylla smaragdina to control lepidopteran citrus pests (Konishi and Ito, 1973); It is also nice to use this recommendation letter to recall and quote the words written in 1752 by the famous Swedish taxonomist, botanist and zoologist, Carl Linnaeus: "Every insect has its predator which follows and destroys it. Such predatory insects should be caught and used for disinfecting crop-plants" (Hörstadius (1974) apud Linnaeus 1752).
Acknowledging the many cases of successes from BPC along our recent history, it is also true that application of BPC strategies during the XX century suffered from wrong-doings, mainly when the introduced biological control agent (BCA, hereafter) was of exotic origin and with a generalist diet-breath; in some cases the release of exotic species resulted on global extinction, reduction in the range of distribution, reduction in the population abundance, and partial displacement, of native and functionally similar species, and interbreeding with them (reviewed in van Lenteren et al. 2006). One of the most famous cases is that of Harmonia axyridis, a coccinellid predator of Asian origin that caused important environmental damage in North America (reviewed in Koch & Galvan, 2008).
Fortunately, after the implementation of the Nagoya protocol (CBD, 2011) importation of exotic species for BPC use was severely restricted and controlled, worldwide. Consequently, companies and agricultural scientist were driven to reinforce their focus and interest on the exploitation of native natural enemies, via the mass-rearing and release of native candidates (augmentative BPC), the conservation of landscapes near the crops to provide resources for natural enemies (i.e. conservation biological pest control), or via the exploitation of the genetic variability of BCAs, to create strains performing better at regulating pest populations under specific biotic or abiotic negative circumstances. Some of these cases are cited in Lartigue et al. (2020). The genetic improvement of BCAs is a strategy still in its infancy, but there is no doubt that the interest for it has significantly increased over the last 5 years (Lommen et al 2017, Bielza 2020, Leung et al 2020).
In my humble opinion, what makes the paper of Lartigue et al. (2020) a remarkable contribution to the field of genetic breeding of BCAs is that it opens a new window of opportunities to the field, by exploring the possibilities for artificial selection of behavioral traits (Réale et al. 2007) to "create" strains of natural enemies displaying behavioral syndromes (Sih et al. 2004) that makes them better at regulating pest populations. The behavioral approach for breeding BCAs can then be extended by crossing it with known abiotic and/or biotic hostile environments (e.g. warm and drought environments, presence of predators/competitors to the BCA, respectively) and engineer strains more prompt to display particular behavioral syndromes to help them to overcome the overall hostility of specific environments. I strongly believe that the approach proposed in Lartigue et al. (2020) will influence the future management of agricultural systems, where strategies including the genetic breeding of BCAs’ behavior will contribute to create better guards and protectors of our crops.

References

Bielza, P., Balanza, V., Cifuentes, D. and Mendoza, J. E. (2020). Challenges facing arthropod biological control: Identifying traits for genetic improvement of predators in protected crops. Pest Manag Sci. doi: https://doi.org/10.1002/ps.5857
CBD - Convention on Biological Diversity, 2011. The Nagoya Protocol on Access and Benefit-sharing, https://www.cbd.int/abs/doc/protocol/nagoya-protocol-en.pdf
Hörstadius, S. (1974). Linnaeus, animals and man. Biological Journal of the Linnaean Society, 6, 269-275. doi: https://doi.org/10.1111/j.1095-8312.1974.tb00725.x
Koch, R.L. and Galvan, T.L. (2008). Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl 53, 23–35. doi: https://doi.org/10.1007/978-1-4020-6939-0_3
Konishi, M. and Ito, Y. (1973). Early entomology in East Asia. In: Smith, R.F., Mittler, T.E., Smith, C.N. (Eds.), History of Entomology, Annual Reviews Inc., Palo Alto, California, pp. 1-20.
Lartigue, S., Yalaoui, M., Belliard, J., Caravel, C., Jeandroz, L., Groussier, G., Calcagno, V., Louâpre, P., Dechaume-Moncharmont, F.-X., Malausa, T. and Moreau, J. (2020). Consistent variations in personality traits and their potential for genetic improvement of biocontrol agents: Trichogramma evanescens as a case study. bioRxiv, 2020.08.21.257881, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: https://doi.org/10.1101/2020.08.21.257881
Leung et al. (2020). Next-generation biological control: the need for integrating genetics and genomics. Biological Reviews, 95(6), 1838–1854. doi: https://doi.org/10.1111/brv.12641
Lommen, S. T. E., de Jong, P. W. and Pannebakker, B. A. (2017). It is time to bridge the gap between exploring and exploiting: prospects for utilizing intraspecific genetic variation to optimize arthropods for augmentative pest control – a review. Entomologia Experimentalis et Applicata, 162: 108-123. doi: https://doi.org/10.1111/eea.12510
Réale, D., Reader, S. M., Sol, D., McDougall, P. T. and Dingemanse, N. J. (2007). Integrating animal temperament within ecology and evolution. Biological Reviews, 82: 291-318. doi: https://doi.org/10.1111/j.1469-185X.2007.00010.x
Sih, A., Bell, A. and Johnson, J. C. (2004). Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology and Evolution, 19(7), 372–378. doi: https://doi.org/10.1016/j.tree.2004.04.009
UUNN. 2015. Transforming our world: the 2030 Agenda for Sustainable Development. report of the Open Working Group of the General Assembly on Sustainable Development Goals (A/68/970 and Corr.1; see also A/68/970/Add.1–3).
UUNN. 2019. World population prospects 2019. United Nations, Department of Economic and Social Affairs, Population Division: Highlights. ST/ESA/SER.A/423.
van Lenteren, J. C., Bale, J., Bigler, F., Hokkanen, H. M. T. and Loomans A. J. M. (2006). Assessing risks of releasing exotic biological control agents of arthropod pests. Annual Review of Entomology, 51: 609-634. doi: https://doi.org/10.1146/annurev.ento.51.110104.151129

The slippersnail (Crepidula fornicata), originally from the eastern coast of North America, has invaded European coastlines from Norway to the Mediterranean Sea [1]. This species is capable of achieving incredibly high densities (up to several thousand individuals per square meter) and likely has major impacts on a variety of community- and ecosystem-level processes, including alteration of carbon and nitrogen fluxes and competition with native suspension feeders [2].

Given this potential for competition, it is important to understand the diet of C. fornicata and its potential overlap with native species. However, previous research on the diet of C. fornicata and related species suggests that the types of food consumed may change with age [3, 4]. This species has an unusual reproductive strategy. It is a sequential hermaphrodite, which begins life as a somewhat mobile male but eventually slows down to become sessile. Sessile individuals form stacks of up to 10 or more individuals, with larger individuals on the bottom of the stack, and decreasingly smaller individuals piled on top. Snails at the bottom of the stack are female, whereas snails at the top of the stack are male; when the females die, the largest males become female [5]. Thus, understanding these potential ontogenetic dietary shifts has implications for both intraspecific (juvenile vs. male vs. female) and interspecific competition associated with an abundant, invasive species.

To this end, Androuin and colleagues evaluated the stable-isotope (d13C and d15N) and fatty-acid profiles of food sources and different life-history stages of C. fornicata [6]. Based on previous work highlighting the potential for life-history changes in the diet of this species [3,4], they hypothesized that C. fornicata would shift its diet as it aged and predicted that this shift would be reflected in changes in its stable-isotope and fatty-acid profiles. The authors found that potential food sources (biofilm, suspended particulate organic matter, and superficial sedimentary organic matter) differed substantially in both stable-isotope and fatty-acid signatures. However, whereas fatty-acid profiles changed substantially with age, there was no shift in the stable-isotope signatures. Because stable-isotope differences between food sources were not reflected in differences between life-history stages, the authors conservatively concluded that there was insufficient evidence for a diet shift with age. The ontogenetic shifts in fatty-acid profiles were intriguing, but the authors suggested that these reflected age-related physiological changes rather than changes in diet.

The authors’ work highlights the need to consider potential changes in the roles of invasive species with age, especially when evaluating interactions with native species. In this case, C. fornicata consumed a variety of food sources, including both benthic and particulate organic matter, regardless of age. The carbon stable-isotope signature of C. fornicata overlaps with those of several native suspension- and deposit-feeding species in the region [7], suggesting the possibility of resource competition, especially given the high abundances of this invader. This contribution demonstrates the potential difficulty of characterizing the impacts of an abundant invasive species with a complex life-history strategy. Like many invasive species, C. fornicata appears to be a dietary generalist, which likely contributes to its success in establishing and thriving in a variety of locations [8].

References

[1] Blanchard M (1997) Spread of the slipper limpet Crepidula fornicata (L. 1758) in Europe. Current state dans consequences. Scientia Marina, 61, 109–118. Open Access version : https://archimer.ifremer.fr/doc/00423/53398/54271.pdf

[2] Martin S, Thouzeau G, Chauvaud L, Jean F, Guérin L, Clavier J (2006) Respiration, calcification, and excretion of the invasive slipper limpet, Crepidula fornicata L.: Implications for carbon, carbonate, and nitrogen fluxes in affected areas. Limnology and Oceanography, 51, 1996–2007. https://doi.org/10.4319/lo.2006.51.5.1996

[3] Navarro JM, Chaparro OR (2002) Grazing–filtration as feeding mechanisms in motile specimens of Crepidula fecunda (Gastropoda: Calyptraeidae). Journal of Experimental Marine Biology and Ecology, 270, 111–122. https://doi.org/10.1016/S0022-0981(02)00013-8

[4] Yee AK, Padilla DK (2015) Allometric Scaling of the Radula in the Atlantic Slippersnail Crepidula fornicata. Journal of Shellfish Research, 34, 903–907. https://doi.org/10.2983/035.034.0320

[5] Collin R (1995) Sex, Size, and Position: A Test of Models Predicting Size at Sex Change in the Protandrous Gastropod Crepidula fornicata. The American Naturalist, 146, 815–831. https://doi.org/10.1086/285826

[6] Androuin T, Dubois SF, Hubas C, Lefebvre G, Grand FL, Schaal G, Carlier A (2021) Trophic niche of the invasive gregarious species Crepidula fornicata, in relation to ontogenic changes. bioRxiv, 2020.07.30.229021, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2020.07.30.229021

[7] Dauby P, Khomsi A, Bouquegneau J-M (1998) Trophic Relationships within Intertidal Communities of the Brittany Coasts: A Stable Carbon Isotope Analysis. Journal of Coastal Research, 14, 1202–1212. Retrieved May 4, 2021, from http://www.jstor.org/stable/4298880

[8] Machovsky-Capuska GE, Senior AM, Simpson SJ, Raubenheimer D (2016) The Multidimensional Nutritional Niche. Trends in Ecology & Evolution, 31, 355–365. https://doi.org/10.1016/j.tree.2016.02.009

How do you estimate the biodiversity of a whole community, or the distribution of abundances and ranges of its species, from presence/absence data in scattered samples?
It all starts with the collector's dilemma: if you double the number of samples, you will not get double the number of species, since you will find many of the same common species, and only a few new rare ones.
This non-additivity has prompted many ecologists to study the Species-Area Relationship. A common theoretical approach has been to connect this spatial pattern to the overall distribution of how common or rare a species can be. At least since Fisher's celebrated log-series [1], ecologists have been trying to, first, infer the shape of the Species Abundance Distribution, and then, use it to predict how many species should be found in a given area or a given number of samples. This has found many applications, from microbial communities to tropical forests, from estimating the number of yet-unknown species to predicting how much biodiversity may be lost if a fraction of the habitat is removed.
In this elegant work, Tovo et al. [2] propose a method that starts only from presence/absence data over a number of samples, and provides the community's diversity, as well as its abundance and range size distributions. This method is simple, analytically explicit, and accurate: the authors test it on the classic Pasoh and Barro Colorado Island tropical forest datasets, and on simulated data. They make a very laudable effort in both explaining its theoretical underpinnings, and proposing a straightforward step-by-step guide to applying it to data.
The core of Tovo et al's method is a simple property: the scale invariance of the Negative Binomial (NB) distribution. Subsampling from a NB gives another NB, where a single parameter has changed. Therefore, if the Species Abundance Distribution is close enough to some NB (which is flexible enough to accommodate all the data here), we can estimate how this parameter changes when going from (1) a single sample to (2) all the available samples, and from there, extrapolate to (3) the entire community.
This principle was first applied by the authors in a previous study [3] that required abundance data in the samples, rather than just presence/absence. Given that binary occurrence data is far more available in a variety of empirical settings, this extension is worthwhile (including its new predictions on range size distributions), and it deserves to be widely known and tested.

ADDITIONAL COMMENTS

1) To explain the novelty of the authors' contribution, it is useful to look at competing techniques.
Some ""parametric"" approaches try to infer the whole-community Species Abundance Distribution (SAD) by guessing its functional form (Gaussian, power-law, log-series...) and fitting its parameters from sampled data. The issue is that this distribution shape may not remain in the same family as we increase the sampling effort or area, so the regression problem may not be well-defined. This is where the Negative Binomial's scale invariance is useful.
Other ""non-parametric"" approaches have renounced guessing the whole SAD: they simply try to approximate of its tail of rare species, by looking at how many species are found in only one (or a few) samples. From this, they derive an estimate of biodiversity that is agnostic to the rest of the SAD. Tovo et al. [2] show the issue with these approaches: they extrapolate from the properties of individual samples to the whole community, but do not properly account for the bias introduced by the amount of sampling (the intermediate scale (2) in the summary above).

2) The main condition for all such approaches to work is well-mixedness: each sample should be sufficiently like a lot drawn from the same skewed lottery. As long as that condition applies, finding the best approach is a theoretical matter of probabilities and combinatorics that may, in time, be given a definite answer.
The authors also show that ""well-mixed"" is not as restrictive as it sounds: the method works both on real data (which is never perfectly mixed) and on simulations where species are even more spatially clustered than the empirical data. In addition, the Negative Binomial's scale invariance entails that, if it works well enough at some spatial scale, it will also work at all higher scales (until one reaches the edges of the sufficiently-well-mixed community)

3) One may ask: why the Negative Binomial as a Species Abundance Distribution?
If one wishes for some dynamical explanation, the Negative Binomial can be derived from neutral birth and death process with immigration, as shown by the authors in [3]. But to be applied to data, it should only be able to approximate the empirical distribution well enough (at all relevant scales). Depending on one's taste, this type of probabilistic approaches can be interpreted as:
- purely phenomenological, describing only the observational process of sampling from an existing state of affairs, not the ecological processes that gave rise to that state.
- a null model, from which everything in practice is expected to deviate to some extent.
- or a way to capture the statistical forces that tend to induce stable relationships between different patterns (as long as no ecological process opposes them strongly enough).

References

[1] Fisher, R. A., Corbet, A. S., & Williams, C. B. (1943). The relation between the number of species and the number of individuals in a random sample of an animal population. The Journal of Animal Ecology, 42-58. doi: 10.2307/1411
[2] Tovo, A., Formentin, M., Suweis, S., Stivanello, S., Azaele, S., & Maritan, A. (2019). Inferring macro-ecological patterns from local species' occurrences. bioRxiv, 387456, ver. 2 peer-reviewed and recommended by PCI Ecol. doi: 10.1101/387456
[3] Tovo, A., Suweis, S., Formentin, M., Favretti, M., Volkov, I., Banavar, J. R., Azaele, S., & Maritan, A. (2017). Upscaling species richness and abundances in tropical forests. Science Advances, 3(10), e1701438. doi: 10.1126/sciadv.1701438

In social species conflicts among group members typically lead to the formation of dominance hierarchies with dominant individuals outcompeting other groups members and, in some extreme cases, suppressing reproduction of subordinates. It has therefore been typically assumed that dominant individuals have a higher breeding success than subordinates. However, previous work on mammals (mostly primates) revealed high variation, with some populations showing no evidence for a link between female dominance reproductive success, and a meta-analysis on primates suggests that the strength of this relationship is stronger for species with a longer lifespan [1]. Therefore, there is now a need to understand 1) whether dominance and reproductive success are generally associated across social mammals (and beyond) and 2) which factors explains the variation in the strength (and possibly direction) of this relationship.
In their preregistration, Shivani et al. [2] plan to perform a meta-analysis on 86 social mammal species to address these two points. More specifically, they will investigate whether the relationship between female dominance and reproductive success vary according to life history traits (e.g. stronger for species with large litter size), ecological conditions (e.g. stronger when resources are limited) and the social environment (e.g. stronger for cooperative breeders than for plural breeders).
The two reviewers and I were particularly positive and enthusiastic about this preregistration and only had minor comments that were nicely addressed by the authors. We found the background well-grounded in the existing literature and that the predictions were therefore clear and well-motivated. The methods were particularly transparent with a nicely annotated R script and the authors even simulated a dataset with the same structure as the actual data in order to make sure that the coding of the data handling and statistical analyses were appropriate (without being tempted to look at model outputs from the true dataset).
Perhaps one limitation to keep in mind once we will have the chance to look at the outcome of this study if that the dataset may not be fully representative of social species with dominance hierarchies. For example, the current dataset contains only one aquatic mammal (Mirounga angustirostris) as far as I can see, which is likely due to a lack of knowledge on such systems. Furthermore, not only mammals exhibit dominance hierarchies and it will be interesting to see if the results of the proposed study hold for other social taxa (and if not, what may explain their differences).
That being said, the proposed study will already offer a much broader overview of the relationship between dominance and reproductive success in animal societies and a better understanding for its variation. The reviewers and I believe it will make an important contribution to the fields of socio-ecology and evolutionary ecology. I therefore strongly recommend this preregistration and we are particularly looking forward to seeing the outcome of this exciting study.

References

[1] Majolo, B., Lehmann, J., de Bortoli Vizioli, A., & Schino, G. (2012). Fitness‐related benefits of dominance in primates. American journal of physical anthropology, 147(4), 652-660. doi: 10.1002/ajpa.22031
[2] Shivani, Huchard, E., Lukas, D. (2020). Preregistration - The effect of dominance rank on female reproductive success in social mammals In principle acceptance by PCI Ecology of the version 1.2 on 07 July 2020. https://github.com/dieterlukas/FemaleDominanceReproductionMetaAnalysis/blob/trunk/PreregistrationMetaAnalysis_RankSuccess.Rmd