Long-term environmental data explain better the abundance of the red octopus (Octopus maya) when testing the niche centroid hypothesis

https://doi.org/10.1016/j.jembe.2021.151609Get rights and content

Highlights

  • An inverse relation between the distance to the niche centroid and abundance exists.

  • Calculation with period averages performed better than monthly data.

  • Period averages may perform better due to seasonal aggregation.

  • Niche centroid distance and abundance relationship can be used as a monitoring tool.

Abstract

Correlative ecological niche models have been widely used to infer the organisms' environmental suitability; nevertheless, the relationship between this estimated suitability and their abundance is less clear. The ecological theory proposes that the internal structure of a species niche determines its abundance. Specifically, abundance should decrease from the niche centroid to its margins (i.e., distance to the niche centroid-abundance hypothesis - DNC-abundance), showing a negative relationship. This study tested this hypothesis using a high-quality dataset of catch per unit of effort as a proxy of the abundance of the red octopus (Octopus maya) collected during its fishing season in the Yucatan Shelf, Mexico in 2012. Species' niche was estimated with half of the abundance data taken as presence-only records and environmental variables that consisted of temperature and salinity. The remaining data were used to analyze the DNC-abundance. The protocol was repeated using the abundance and environmental data corresponding to each month of the fishing season. The effect of estimating the species niche was also examined using two different environmental datasets: one that matched abundance in a more finely temporal resolution (average values of the corresponding month in 2012 at a resolution of 9 km2) versus another one with a coarser temporal resolution (long-term data: salinity [1955–2006] and temperature [2002−2010] at a resolution of 1 km2). A consistent inverse relationship was found between abundance and distance to the centroid for the most evaluated scenarios, suggesting that niche structure could be informative for fishery monitoring even under climate change scenarios. In addition, contrary to our expectations, relationships were stronger when the coarse temporal resolution variables were used, which suggests that longer temporal environmental conditions may determine population abundance, probably due to seasonal aggregation in the western region of the Yucatan Peninsula.

Introduction

Hutchinson originally conceived the niche as a hypercube in a multivariate environmental space representing an organism's potential tolerance (Hutchinson, 1957). He also suggested an “optimal” region of the niche where conditions for survival are maximized (Holt, 2009). This idea was later adopted and extended by Maguire (1973) describing the niche as an ellipsoid in correspondence with many experimental studies of organism physiology (Biggs and McDermott, 1973; Birch, 1953; Blaszkowski and Moreira, 1986; Haefner, 1969; Hooper et al., 2008; Rothlisberg, 1979). Maguire (1973) stated that different regions of the ellipsoid-like niche structure correspond to different carrying capacities (K) and intrinsic growth rates (r) of populations, and in the center of the ecological niche is where environmental conditions are optimal for populations. In this region, K and r are maximized, potentially allowing populations to achieve higher abundances or densities (Fig. 1).

Brown (1984) admitted the impossibility of considering the influence of environmental variables on population attributes due to the difficulty of obtaining the necessary inputs, which was one significant issue decades ago. Nowadays, environmental data and biological information are widely available because of large scale digitization of data that allows public access to species presence records and environmental information (Soberón and Peterson, 2004). In contrast to the idea that abundance should decrease with the distance to the center of the geographic distribution (geographic-abundance hypothesis Brown, 1984), the highest abundance should occur in the center of the niche, and as populations get farther away from it, abundance decreases (Martínez-Meyer et al., 2013; Yañez-Arenas et al., 2012). This expected negative relationship is usually denominated as the distance to the niche centroid-abundance hypothesis (DNC-abundance), and it is currently a hot topic in the field of ecological niche modeling (Yañez-Arenas et al., 2020).

For instance, Martínez-Meyer et al. (2013) found a consistent negative DNC-abundance relationship across different species of terrestrial vertebrates. This relationship should not be casual since the DNC-abundance represents the species' fundamental niche internal structure. While some studies have provided empirical support to this hypothesis (Escalante and Martínez-Meyer, 2013, Martin et al., 2016, Martínez-Gutiérrez et al., 2018, Osorio-Olvera et al., 2020b, Ureña-Aranda et al., 2015, Yañez-Arenas et al., 2014b), others have found weak or no support at all (Dallas et al., 2017; Dallas and Santini, 2020; Santini et al., 2019). However, on the one hand, low quality of occurrence data due to sampling bias (Knouft, 2018, Yañez-Arenas et al., 2014a), low pixel resolution (multiple abundance data points falling within a single climate pixel losing environmental information), or inappropriate methodological decisions (e.g., the use of convex hull to represent the niche) (Soberón et al., 2018) can obscure the relationship, even if it exists (Osorio-Olvera et al., 2020b; Osorio-Olvera et al., 2019; Soberón et al., 2018). On the other hand, processes like transitory states, the heterogeneous spatial structure of suitability, Allee effects (Osorio-Olvera et al., 2020b), and unfilled niches due to biotic or dispersal limitations (Soberón and Nakamura, 2009; Soberón and Peterson, 2005; Yañez-Arenas et al., 2020) would break down the expected relationship.

In addition, under the usual modeling approach, the ecological niche is estimated using environmental layers that consist of long-term yearly or monthly averages (defined here as “coarse temporal resolution” - CTR). Although these approaches are helpful, a problem not traditionally considered arises, the environmental conditions do not accurately match occurrence dates. Such procedures could influence niche estimations reducing the DNC-abundance relationship, especially in climates with marked seasonal differences. The proposal in this study is that if the occurrences and environments had a higher temporal match (defined here as “finer temporal resolution” - FTR), the DNC-abundance relationship might increase if compared to the CTR. To our knowledge, no previous work related to DNC-abundance has reviewed the effect of the temporal match between environmental and occurrence data.

Therefore, the objective of this research is to test the viability on the DNC-abundance hypothesis on an endemic holobenthic marine organism of commercial importance in the Yucatan Shelf, Mexico – the red octopus (Octopus maya Voss and Solís-Ramírez, 1966). Additionally, a second goal is to compare the FTR and CTR datasets of environmental variables for estimating the species' niche. It is important to highlight that a critical assumption needed to test the DNC-abundance hypothesis is fulfilled in the case of this species. That is, presence and abundance records span most of their entire geographic range (Osorio-Olvera et al., 2020b). Thus, this study anticipates finding a negative correlation between the niche centroid and the red octopus abundance.

Conceivably, if environmental heterogeneity exists in the Yucatan Shelf, the DNC-abundance relationship will be more reliable than if conditions are homogenized since no area should be preferred. If a link can be found between the DNC-abundance hypothesis, understanding the processes that determine the spatio-temporal patterns of the species abundance may increase. In turn, the description of this relationship could help predict the impact of threats, such as climate change, redirecting the predictions to catch potential instead of only suitability values. It would be very important, especially in heat-sensitive species of commercial importance, such as the red octopus (Juárez et al., 2015; Pascual et al., 2019; Sanchez-García et al., 2017).

Section snippets

Study area

The Yucatan Peninsula (YP) is a biogeographical province placed in southeast Mexico that has an extensive continental shelf with a gentle slope (Monreal-Gómez et al., 2004). The region is formed by three Mexican states (Campeche, Yucatán, and Quintana Roo), Belize, and part of Guatemala and divides the Gulf of Mexico from the Caribbean Sea. Generally, in the western region of the YP, the temperature varies from 21 °C in January to 30 °C in September with oscillations up to 4 °C in a summer day (

Fishing season data

A total of 76,043 octopuses were collected from ~1162 fishing trips during the fishing season. The months with the highest numbers of total catches and CPUE by fishing trip were obtained in August and September, while the lowest ones were obtained in November and December (Fig. 3A). The environmental conditions associated with the presence of the red octopus varied between the two temporal resolution datasets of variables (Fig. 3B). For the CTR dataset, individuals are found at temperatures and

Discussion

Our results show that generally, the highest abundance tends to be found near the centroid of the ellipsoid; therefore, as occurrences move further away from the centroid, the potential abundance diminishes, coinciding with what has been reported in other studies (Martínez-Meyer et al., 2013; Osorio-Olvera et al., 2020b; Ureña-Aranda et al., 2015). It is important to point out that the relationships were mainly driven by the right-skewed distribution of the data at low distances of the niche

Conclusions

The DNC-abundance hypothesis may be a helpful tool to understand how environmental variables may control abundance patterns in marine organisms of commercial importance as it has been similarly seen in reef fishes around the world (Waldock et al., 2019). However, if this tool is used in fisheries, environmental variables that can be easily interpreted should be used, especially for climate change scenarios. Moreover, the pixel size should have enough resolution to describe the DNC-abundance

Declaration of Competing Interest

The authors declare that they have no known competing financial interestsor personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This study is the result of a Graduate Studies Doctoral degree thesis at Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México (UNAM); the authors are grateful to UNAM and to the Consejo Nacional de Ciencia y Tecnología (CONACYT) for the scholarship funding the development of this research and D.Fischer for English edition. All the data for the red octopus used in this study was obtained from the projects: “Patrones de movimiento y de distribución espacio temporal del pulpo

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