Macrobrachium olfersii (Wiegmann, 1836)

Santos, Rafael Carvalho, Nogueira, Caio Santos, Jaconis, Milena Silva, Davanso, Thiago Maia, Costa, Rogerio Caetano & Hirose, Gustavo Luis, 2022, New Insights into the Male Morphotypes of the Amphidromous Shrimp (Weigmann, 1836) (Caridea: Palaemonidae) and a Discussion on Social Dominance Hierarchies., Zoological Studies 61 (83), pp. 1-18 : 11-14

M. olfersii morphotypes descriptions

In the recent study by Rossi et al. (2022), the same amount of male morphotypes was found for M. olfersii compared to the present study, which highlights the importance of analyzing the variation of different populations of the same species. Nevertheless, the application of the morphotypes studies in a single population may help to improve the knowledge about this feature in M. olfersii , since it will not only confirm the presence of distinct males morphotypes, but also avoid any bias that could be present by possible distinct local variations of different populations. It is important to highlight that a minute description for each morphotype is necessary, to prevent possible doubts in the morphotypes separation that may arise. By carrying out this detailed description, it is possible to reduce, or even suppress the description of subtypes (transitional morphotypes), such as the once observed for M. rosenbergii , which previously 5 morphotypes were described, but only three remains due two of them were rectify as subtypes ( Kuris et al. 1987). In addition, the use of a robust description, will help in future studies that aim to approach some biological and ecological features in the three morphotypes of M. olfersii .

Another relevant aspect is the presence of juveniles, since they are the previous morphological distinction before the M1. By using these demographic categories, and separating them from the adults using the sexual maturity, we were able to access the observed overlap that occurs in the carapace length (CL) among the juveniles and the morphotypes. Thus, this demonstrates the importance of the morphometry of the cheliped and the morphology of the propodus, as well as the detailed ornamentation description in the separation of the distinct morphotypes of M. olfersii . We emphasize the importance of conducting behavioral studies to truly understand the dominance that exists between these male morphotypes and the size variations that occur among them, that will bring more support to the described here and by Rossi et al. (2022).

Population structure studies of M. olfersii support the occurrence of representatives of the morphotypes described in the present study. These studies have reported significant variations in the size of chelipeds, mainly among males of different size classes ( Lombardi et al. 1996; Ammar et al. 2001; Mossolin and Bueno 2002 2003; Pescinelli et al. 2016). Our result reinforces that the presence of morphotypes is a common feature in some species of this genus as mentioned by Moraes-Riodades and Valenti (2004). In addition to the eight species with different morphotypes already described, at least 19 other species are also expected to present this characteristic according to behavioral observations carried out on the interaction of males ( Karplus and Barki 2019).

Some males of Macrobrachium have an exaggerated development of chelipeds. Generally, they have a mating system called “mate guarding”, in which males are larger than females and have overdeveloped chelipeds that are used as weapons. All caridean species that have described male morphotypes presumably have this type of mating system ( Correa and Thiel 2003; Thiel et al. 2010; Bauer and Thiel 2011; Bauer et al. 2014; Karplus and Barki 2019). Alternatively, some species of the same genus also present a mating system called “pure search”, in which females are larger than males. These species do not have overdeveloped chelipeds and do not present any type of agonistic behavior to gain access to sexual partners ( Correa and Thiel 2003; Bauer and Thiel 2011). Therefore, some species of Macrobrachium do not have male morphotypes, specifically in the case of species that have the “pure search” mating system. In these species, there is no abrupt variation in total length and morphology of chelipeds, as happens in M. jelskii (Miers, 1878) and M. pantanalense Dos Santos, Hayd & Anger, 2013 ( Nascimento et al. 2020; Nogueira et al. 2022a).

On the other hand, species that have morphological and behavioral characteristics that indicate the presence of morphotypes may still not have the exaggerated development of chelipeds. This is the case for M. iheringi (Ortmann, 1897) ( Nogueira et al. 2019 2022b). In the same way, there may be a variation in populations of species whose attributes have already been reported, demonstrating the absence of morphotypes in specific populations, such as in M. amazonicum ( Pantaleão et al. 2012; Paschoal et al. 2019; Silva et al. 2019). This variation between the non-occurrence of morphotypes in some species or only in specific populations may be related to different factors, such as regulations in the production of peptides due to the small size of the androgenic gland ( Rocha and Barbosa 2017; Paschoal and Zara 2019), or by environmental factors ( Maciel and Valenti 2009), e.g., nutrients available in the environment, availability of shelters, temperature, and social growth control. Another possibility is related to selective sampling ( Santos et al. 2016; Rios et al. 2021), by excluding the variety of size classes, i.e. picking only smaller individuals.

The Amazon River shrimp ( M. amazonicum ) is the only species so far that may or may not have populations with distinct male morphotypes. Most populations that have morphotypes have been reported in rivers with access to the estuary ( Nogueira et al. 2020), while those that do not have distinct male morphotypes are in exclusively freshwater environments ( Pantaleão et al. 2012; Paschoal et al. 2019; Silva et al. 2019). In populations of this species without distinct male morphotypes, females are larger than males and present characteristics of the “pure search” mating system. Therefore, these populations need to be analyzed with caution. A study by Anger (2013) reported the possibility that specific populations of M. amazonicum from isolated estuarine regions, or those that do not present morphotypes, may belong to another species. These populations of M. amazonicum with such characteristics may be M. pantanalense , especially because they are found in environments outside its type locality ( Vergamini et al. 2011; Calixto-Cunha et al. 2021), and present high morphological similarity and genetic proximity to M. amazonicum ( Vergamini et al. 2011; Robe et al. 2012). Thus, we recommend that future studies that address populations of M. amazonicum that are located in the central-west, southeast, and south regions of Brazil and that present only small males use molecular methods to assist in species identification.

Most Macrobrachium species with the presence of distinct male morphotypes present characteristics decisive for their identification ( Kuris et al. 1987; Moraes-Riodades and Valenti 2004; Rojas et al. 2012; Nogueira et al. 2020; Rios et al. 2021; Vargas-Ceballos et al. 2021). These characteristics are mostly represented by the size, color, morphology of the cheliped, and body size variation (though the body size characteristic is not always observed) ( Holthuis 1950 1952). Although there is no marked difference in carapace length between the three described morphotypes of M. olfersii , cheliped length varies significantly, mainly between M3 and the other morphotypes. This pattern was also found for M. acanthurus , M. amazonicum , and M. rosenbergii ( Kuris et al. 1987; Moraes-Riodades and Valenti 2004; Rios et al. 2021). This shows that body size does not establish a hierarchical pattern between morphotypes, since in many cases there is an overlap in carapace length among these groups. This reinforces the importance of chelipeds in the discrimination of male morphotypes and in the establishment of dominance among morphotypes, since this structure is essential for the success of dominant individuals during fights ( Barki et al. 1992 1997; Karplus 2005).

Morphometry of the major cheliped

The allometric coefficients observed in the three male morphotypes and in juveniles of M. olfersii indicate a difference between M3 and the other groups. M3 is the only group that presents an isometric development of all the articles that constitute the major cheliped of the second pair of pereopods. The other groups have mostly shown negative allometry in the development of these structures. Furthermore, the slope values showed an increase from M1 to M3, demonstrating the importance of chelipeds in the categorization of social dominance hierarchies in Macrobrachium . This change in the larger morphotype configures a greater investment in the development of the major cheliped. This structure is more frequently used to strongly squeeze opponents during fights, so dominant males have advantages over submissive males, facilitating access to better resources, such as territory, food, and sexual partners (Conover and Milner 1978; Mariappan et al. 2000).

There was a high overlap in carapace length between male morphotypes and even in juveniles. There were small dominant males with CL similar to large juveniles. However, when we compare the cheliped length of these same individuals (smallest M3 and largest juvenile), we observed that this structure in M 3 males was twice the size than in juveniles. This indicates differential investment in the development of chelipeds by the dominant individuals, even in cases where animals are small (CL). Due to this high overlap in CL among the male morphotypes, we can assume that the transition from one morphotype to another in M. olfersii occurs in just one molt, as was suggested for M. amazonicum ( Pantaleão et al. 2014) . Many factors can influence the transition between morphotypes, the main one being the presence or absence of a dominant male at the site. These individuals are known to occupy a specific area in the environment, and when the dominant male dies or loses its weapon, another individual usually starts to grow at a higher rate and becomes the dominant one ( Karplus and Barki 2019; Ibrahim et al. 2021; Vargas-Ceballos et al. 2021).

Chelipeds morphology and propodus shape

The morphology of chelipeds varies in M. olfersii , mainly regarding spines, presence of pubescence, and propodus shape. The amount and arrangement of spines varying among morphotypes are expected in Macrobrachium ( Moraes-Riodades and Valenti 2004; Nogueira et al. 2020; Rios et al. 2021), since these structures are used in agonistic behavior, being considered defensive ornamentation ( Moraes-Riodades and Valenti 2004). In M. olfersii , the number of spines, as well as their angulation, is evidently higher in M3, another diagnostic feature for the identification of this morphotype. These characteristics (amount and angle of spines) may be related to the frequency of disputes that occur between dominant male, which may increase the damage caused to opponents during fights ( Thiel et al. 2010; Rojas et al. 2012; Bauer et al. 2014; Nogueira et al. 2021).

The presence of pubescence in chelipeds is also a feature used to separate the morphotypes of M. olfersii . This ornamentation, despite being common in dominant morphotypes of some Macrobrachium species, was included as a comparative parameter only among the morphotypes of M. acanthurus ( Rios et al. 2021) , as the authors suggested there was a relationship between this structure and reproductive fitness. In M. grandimanus , a characteristic similar to pubescence in the claws was also recorded, being the presence of a patch of setae on the propodus of dominant morphotypes ( Wortham and Maurik 2012). As in M. acanthurus , this pubescence of M. olfersii morphotypes may play chemoreceptor functions for the perception of mating-receptive females ( Altner et al. 1983). Another hypothesis is that these structures can serve as a visual signal from dominant to submissive individuals to establish dominance without a direct fight. The presence of pubescent setae on the cheliped lets this structure appear larger than it actually is, inhibiting potential competitors ( Wortham and Maurik 2012). In M. olfersii , this can be represented not only by the presence of pubescence but also by the difference found in the propodus shape between the male morphotypes, a structure that is more robust in M3.

The geometric morphometric analysis demonstrated that this tool can be effective in identifying and separating male morphotypes in shrimp species by evaluating whether the differences observed between the propodus shape are significant. A variation in the shape of this structure was observed among morphotypes of M. olfersii , showing an increase in the palm region of the propodus of M3, which is more robust and wider, while the fixed finger is shorter and more robust, in comparison to M1 and M2, being a pattern similar to that observed between the propodus shape of the morphotypes Açu and Mirim of M. brasiliense ( Nogueira et al. 2020) . The more robust shape of the propodus in M3 means that this structure can generate more force than the propodus of subordinate morphotypes since a larger propodus can accommodate more muscle mass ( Levinton et al. 1995; Palaoro et al. 2020). Therefore, the dominant morphotypes are likely to be able to squeeze their opponents more tightly than the other morphotypes, helping these organisms to maintain dominance over submissive males.