An intra-continental invasion of the temperate freshwater copepod Skistodiaptomus pallidus (Herrick, 1879) (Calanoida, Diaptomidae) in tropical Mexico

The freshwater planktonic calanoid copepod Skistodiaptomus pallidus (Herrick, 1879), native to cold and temperate latitudes in the United States, has recently been identified as having non-indigenous populations in Western Europe and New Zealand. A further non-indigenous population of this species is recorded here from a large inland reservoir in the State of Sinaloa, northwestern Mexico. This copepod species can be distinguished from its congeners mainly by its pincer-like distal process of the second exopodal segment of the right fifth leg of the male. This is the first record of S. pallidus in tropical latitudes and its presence in Mexico is far outside of its known intra-continental range. This introduction is attributed to human agency and deemed as a recent arrival. The local fisheries and aquaculture activities in the surveyed reservoir are the most probable vectors of this introduction but avian transportation by migrating pelicans is also possible. Because of the competitive abilities of this species and the connectivity of this reservoir, it is expected that S. pallidus will spread to other man-made locations in Mexico.

Skistodiaptomus pallidus is relatively widely distributed, having spread across the coldtemperate areas of the United States (Byron and Saunders 1981), but it is largely restricted to latitudes north of the 30°N.This species has been regarded as native to the north-central plain states of the United States, northeast to New York and in states in the Mississippi River basin, Montana, Wisconsin, Michigan, Georgia, Texas, and west to Colorado (Pennak 1989;Torke 2001;Thum and Stemberger 2006).This calanoid copepod has been recognized as a nonindigenous species outside of the United States, with recent records in New Zealand and Germany (Duggan et al. 2006;Brandorff 2011).
The freshwater copepod fauna of Mexico has been investigated in different regions (Suárez-Morales and Reid 1998;Elías-Gutiérrez et al. 1999;Suárez-Morales et al. 2010)   The taxonomical examination of this material resulted in the identification of S. pallidus.Because there are few taxonomical illustrations of this species, we present complementary morphological data about this copepod, particularly in reference to the male fifth leg.The record of this species is presented herein as an accidental introduction to this system in an area well outside the known distribution of the species.We discuss the probable route of introduction to the surveyed area.

Material and methods
Adult males and females of Skistodiaptomus pallidus were collected during a biological survey of the El Comedero reservoir.The study aimed to determine the composition, diversity, and distribution of the freshwater zooplankton of this large reservoir that is used for fishing and aquaculture (Beltrán 2003).Zooplankton was collected bi-monthly throughout 2010 using a Wisconsin-type plankton net with a mesh size of 90 µm.Samples were fixed and preserved with 4% formalin solution.Copepods were sorted and transferred to 70% ethanol for preservation and storage.The taxonomic analysis of the copepods involved dissection of appendages, preparation of microscope slides using glycerol as a mounting medium, and illustrations prepared with the aid of a camera lucida.
The José López Portillo reservoir, also known as El Comedero, is located in the municipality of Cosala in the state of Sinaloa, northwestern Mexico (Figure 1).The area is crossed by two important rivers: the San Lorenzo and the Elota.The former river flows through the county of Cosala, enters the municipality of Culiacan, and flows into the Pacific Ocean.The reservoir has a catchment area of 8 919 km 2 and has an average annual runoff of 1 572 million m 3 .To take advantage of this important hydrologic basin the El Comedero reservoir has a total capacity of 3 399 million m 3 , being the fourth largest in the state.Conductivity of El Comedero reservoir water ranges from 142 to 203 μS cm -1 , temperature between 21.9 (January) and 31.2°C(July), and dissolved oxygen between 5.5 (January) and 8.7 mg/l (September).

Physical and chemical conditions
During sampling of zooplankton in March 2010 the water temperature was 23.5°C, conductivity 142 μS cm -1 , oxygen 7.6 mg/l, and pH was 8.1.Chlorophyll a concentration in this month was the lowest of the year at 0.33 μg l -1 .

Discussion
Only one other species of the genus Skistodiaptomus has been recorded from the Neotropical region, S. oregonensis (Suárez-Morales and Reid 1998; Dussart and Defaye 2002).Skistodiaptomus oregonensis cannot be confused with S. pallidus because of the peculiar pincer-like structure of the distal exopodal segment of the right male fifth leg (Figure 3G), among other characters.Hence, it is confirmed here that the non-indigenous diaptomid copepod S. pallidus is present in northwestern Mexico.The body size of both females and males is as reported by Brandorff (2011).Based on genetic and molecular studies, Thum and Derry (2008) stated that there are at least four different lineages currently contained in the nominal species S. pallidus.However, the reproductive isolation among populations has not been tested and there are no morphological characters known to reflect these lineages; in any case, the presence of any one of these presumed lineages in Mexico is unexpected.
The biogeography of S. pallidus in North America was described by Byron and Saunders (1981) as historically occurring primarily in the central sector of the United States and the Mississippi Valley states with a recent expansion into the northeastern United States resulting from the construction of numerous artificial aquatic systems.A different pattern was  proposed by Stemberger (1995)  Therefore, based on this information, and pending the results of samplings in natural and man-made systems of adjacent areas, it is speculated that the population of S. pallidus found in the surveyed area invaded this manmade system recently.The physical and chemical conditions at El Comedero differ from the usual range reported for S. pallidus; this species usually inhabits betamesotrophic (with intermediate productivity levels) to eutrophic habitats but the surveyed area is a highly oxygenated oligotrophic system, with relatively low values of phosphorus PO 4 (0.02-0.20 mg l -1 ), nitrogen (NO 2 : 0.001-0.023mg l -1 , NO 3 : 0.132-0.176mg l -1 ), and chlorophyll a (0.33-1.72 μg l -1 ).In addition, S. pallidus is known to prefer cool waters <12°C.However, the temperature was 24° when this species was collected in El Comedero.The pH and conductivity ranges recorded at El Comedero are both within the range of this copepod (7.5-8.6 and 77-660 μS cm -1 , respectively) (Kipp and Benson 2010).
This species has been hitherto recorded mainly from high, cold-temperate latitudes in North America (e.g.Montana 46°N, Ontario 43°, Lake Tahoe 39°), and as an introduced species in Germany (53°N) and New Zealand (37°S).The southernmost records in North America are from Mississippi, Texas, and Georgia (30-32°N) (Duggan et al. 2006;Thum and Derry 2008;Brandorff 2011).This is the first record of S. pallidus from tropical areas, at latitudes below 30°N; it is recorded herein at 24°N in northwestern Mexico.This is also the first diaptomid copepod known as an invader in Mexico; several Nearctic species of diaptomids are known to be distributed in Mexico as a result of natural dispersal and processes of radiation including post-glacial stranding (Granados-Ramírez and Suárez-Morales 2003;Suárez-Morales et al. 2005) but the disjunct distribution of S. pallidus (the nearest record along the Pacific coast is Lake Tahoe), and the fact that the species is well outside of its known climate regime and latitudinal range, suggest that it represents an intra-continental introduction of a Nearctic diaptomid species into a fully tropical zone.The tropical diaptomid Arctodiaptomus dorsalis (Marsh) shows the opposite pattern of introduction; it had not been previously recorded north of Florida in North America until Reid (2007) reported it from temperate latitudes in the United States.It is also expected that S. pallidus will spread to other areas of northern and central Mexico because of its ability to spread using human mediated transport vectors and its highly competitive features.Skistodiaptomus pallidus is an efficient predator, consumes algae, and can become cannibalistic when resource availability is low (Williamson and Vanderploeg 1988).This latter point may be important in the oligotrophic conditions of El Comedero.Overall, S. pallidus commonly becomes dominant in invaded systems over local species (Byron and Saunders 1981), but this is known only for nontropical latitudes.Hence, the potential impact of this highly competitive temperate copepod is unpredictable when it is introduced to tropical communities.
One possible vector for introduction of copepods to new areas includes dispersal via migrating birds (Reid and Reed 1994;Green and Figuerola 2005).There are reports of passive dispersal of copepods by avian transport in North America generally involving the southward migration of northern species (Saunders et al. 1993).Diapausing eggs have been reported for S. pallidus (Dowell 1997) It is well known that human activities related to aquaculture and shipping are major vectors for the dispersal of aquatic organisms (Holeck et al. 2004;Wonham et al. 2005).The only case in which the vector of this invasive diaptomid has been identified is in New Zealand, where S. pallidus was introduced via dumping of aquarium contents wherein present as live food (Duggan et al. 2006).Ballast water is yet another possibility of introduction, but because of the distance between the coastline and the El Comedero reservoir (80 km), it is unlikely that S. pallidus was introduced this way, as reported by Brandorff (2011) on the German coast.In different geographic areas of North America, the introduction of S. pallidus has been attributed to handling of bait buckets, fishing equipment, by recreational boaters, with hatchery stock, or through natural dispersal (Mills et al. 1993;Reid and Hudson 2008).In Sinaloa, Mexico the activities related to fishery and hatchery stocks probably represent sources of introduction although aquarium live food cannot be discarded as a vector.The reservoir is intensively used for fish culturing, including the tilapia Oreochromis aureus (Steindachner, 1864), the channel catfish Ictalurus punctatus (Rafinesque, 1818), and the largemouth black bass Micropterus salmoides (Lacépede, 1804).The local activities linked to aquaculture and fisheries, including live food, hatchery stock incorporation, and aquarium products are thus proposed as the probable vector of this introduction.

Figure 1 .
Figure 1.Geographic location of the El Comedero reservoir in Sinaloa, Mexico, the site where Skistodiaptomus pallidus was recorded.

Figure 3 .
Figure 3. Skistodiaptomus pallidus.Adult male from Sinaloa, Mexico.A. habitus, dorsal view; B. right geniculate antennule; C. detail of antennular segments 10-13; D. detail of last antennular segment; E. fifth legs; F. detail of endopod of left fifth leg; G. detail of left fifth leg showing ornamentation of segments.
, and this diaptomid is potentially able to survive transportation in this manner.The American white pelican Pelecanus erythrorhynchos Gmelin, 1789 breeds in areas of north-central and western United States.It spends the late fall and winter in different regions of Mexico (Mendoza-Salgado et al. 2011) and may be a suitable vector for diapausing eggs of S. pallidus.Populations of this pelican are known to dwell at El Comedero during fall and winter.